LWT - Food Science and Technology 129 (2020) 109507

Contents lists available at ScienceDirect

LWT - Food Science and Technology

journal homepage: www.elsevier.com/locate/lwt

Thermal inactivation of Salmonella enterica in Philippine flowing-type T

peanut butter
Mark Anthony B. Pelaez∗, Gerieka R. Anapi, Donna V. Bautista, Ma. Dulce P. Dallo,
Joseph Conrad M. Libunao, Alonzo A. Gabriel
Laboratory of Food Microbiology and Hygiene, Department of Food Science and Nutrition, College of Home Economics, Alonso Hall, Antonio Ma. Regidor St., University of
the Philippines Diliman, Quezon City, 1101, Philippines

A R T I C LE I N FO A B S T R A C T

Keywords: To the investigators’ knowledge, this is the first time that the thermal death behavior and kinetics of S. enterica in
Peanut butter Philippine flowing-type peanut butter is being reported. A seven-strain cocktail of S. enterica serovars was in-
Salmonella enterica oculated in peanut butter and was allowed to pre-adapt to the food matrix for 24 h prior to heat inactivation
Thermal inactivation studies. Results showed that the organism generally exhibited a log-linear heat inactivation behavior
D-value
(R2 > 0.90). Thermal resistance decreased with increasing heating temperature. The decimal reduction times
Z-value
determined were D60 = 47.98 min, D65 = 40.07 min, D70 = 31.23 min, D75 = 25.54 min, and D80 = 16.15 min.
The z-value determined for the test organisms in peanut butter was 44.50 °C. These results confirm the high
thermal resistance of S. enterica in peanut butter medium and can be used as baseline data in the establishment of
supplementary heat treatment for locally-produced peanut butter.

1. Introduction
Salmonella is the most common cause of foodborne diseases globally
because of its ubiquitous nature, resistance under adverse environ-
mental conditions, and low infectious dose (Finn, Condell, McClure,
Amézquita, & Fanning, 2013). Although outbreaks of Salmonella in-
fections are traditionally associated with fresh produce and animal
products, foods with low water activity such as peanut butter have been
increasingly implicated (CDC 2009; Sánchez-Maldonado, Lee, & Farber,
2018; Sheth et al., 2011). Since 2005, there have been three multistate
Salmonella outbreaks associated with commercial peanut butter that
resulted in hospitalizations and product recalls in the United States. The
most recent outbreak occurred in 2012 involving 42 persons from 20
states being infected with the outbreak strain of Salmonella Braedeney
(CDC, 2012). The causative strain for this salmonellosis matched with
environmental and unopened product isolates from the processing fa-
cility of the manufacturer (CDC, 2013). In 2009, there were 714 persons
infected with Salmonella Typhimurium from 46 states (CDC, 2009). The
peanut butter product implicated in this outbreak was sold only to in-
stitutional clients, hence the relatively large number of cases. Pre-
viously, 715 persons from 48 states had been infected with Salmonella
Tennessee (CDC, 2007; Sheth et al., 2011). In the Philippines, a recall
for several batches and variants of a locally-produced peanut butter was
also ordered by the Food and Drug Administration in 2009 when sev-
eral market samples tested positive for Salmonella (Merueñas, 2009). In
2014, another local distributor initiated a voluntary recall of different
batches of peanut butter due to possible Salmonella contamination
(Herriman, 2014).
The main causes of Salmonella contamination are poor sanitation
practices, substandard facilities, faulty equipment, defective pest con-
trol, lack of a functional Good Manufacturing Practices (GMPs), and
poor ingredient control (Podolak, Enache, Stone, Black, & Elliott,
2010). Peanuts can be contaminated at any point during cultivation,
harvest, transportation, and storage (Kilonzo-Nthenge, Rotich, Godwin,
& Huang, 2009). Since roasting is typically done at 160–200 °C for
20–50 min (USEPA, 2009), subsequent post-roasting steps are the most
plausible points of entry for contaminating pathogens (Ma et al., 2009).
Cross-contamination during processing can easily result from poor
equipment sanitation as with the case of the 2012 US outbreak (USFDA,
2012). Typical grinding and packaging of roasted peanuts occurs at
48 °C (Woodroof, 1983) but the inactivation of microorganisms in
peanut butter is minimal at this temperature (Mattick et al., 2001). It
has been reported that a 6-log CFU/g reduction in Salmonella was
achieved only after more than 50 min heat treatment at 85 °C (Keller

∗
Corresponding author. Laboratory of Food Microbiology and Hygiene, Department of Food Science and Nutrition, Teodora Alonso Hall, College of Home
Economics, A. Ma. Regidor Street, University of the Philippines, Diliman Campus, 1101, Quezon City, Philippines.
E-mail address: mbpelaez@brc.pshs.edu.ph (M.A.B. Pelaez).

https://doi.org/10.1016/j.lwt.2020.109507
Received 5 December 2019; Received in revised form 24 April 2020; Accepted 25 April 2020
Available online 18 May 2020
0023-6438/ © 2020 Elsevier Ltd. All rights reserved.
M.A.B. Pelaez, et al.
et al., 2012), which supports previous findings of the high thermal re-
sistance of Salmonella (Ma et al., 2009; Shachar & Yaron, 2006). These
findings suggest that the current processing of peanut butter may not
always include an effective pathogen-elimination step and that post-
process contamination such as during repacking may lead to foodborne
infections (Kilonzo-Nthenge et al., 2009). This presents a serious food
safety challenge since the survival of Salmonella in peanut butter during
prolonged storage is well-documented (Burnett, Gehm, Weissinger, &
Beuchat, 2000; He, Guo, Yang, Tortorello, & Zhang, 2011; Kilonzo-
Nthenge et al., 2009).
Pathogen inactivation by thermal treatment of peanut butter in its
finished packaging has recently been explored either as an additional
pathogen control measure (Li, Huang, & Chen, 2014; Song & Kang,
2016) or as a reconditioning step (Wright, Minarsich, Daeschel, &
Waite-Cusic, 2017). However, the high fat content and low water ac-
tivity of these products provide protection to microorganisms from
what would otherwise be highly effective food processing technologies
(He et al., 2011). The heat resistance of Salmonella spp. is significantly
influenced by product formulation (He et al., 2011; Kataoka et al.,
2014; Li et al., 2014; Ma et al., 2009; Shachar & Yaron, 2006). For
instance, reduced fat formulations with increased carbohydrate content
requires significantly longer treatment times to achieve a 5-log reduc-
tion of Salmonella spp. compared to standard peanut butter formula-
tions (He et al., 2011; Li et al., 2014). Although Salmonella spp. are
ordinarily sensitive to heat, the cells can become heat resistant in dry
food products such as peanut butter (Deng, Li, & Zhang, 2012; Fong &
Wang, 2016; Gruzdev, Pinto, & Sela, 2011; Li et al., 2014). This phe-
nomenon of cross-adaptation is of particular importance considering
that contaminating pathogens in the peanut butter processing en-
vironment have most likely been exposed and pre-adapted to desicca-
tion stress.
Given the variability in thermal resistance of Salmonella spp. in
different peanut butter product formulations, it is necessary to evaluate
the efficacy of heat treatment in different variants of peanut butter. In
the Philippines, locally-produced peanut butter products are usually
non-stabilized and have higher sugar contents of 10–20 g per serving
(Galvez, Francisco, Lustre, & Resurreccion, 2006) relative to the USDA
standard (USDA, 2018). This study was conducted to determine the
thermal inactivation kinetics (DT- and z-values) of Salmonella enterica in
local peanut butter after pre-adaptation to low water activity. To the
best of the investigators knowledge, this is the first time that the
thermal inactivation behavior and inactivation kinetics of S. enterica is
being reported in Philippine flowing-type peanut butter. The results
obtained in the study may be used in the establishment of thermal
process schedule for the tested commodity to ensure safety from the
pathogen.
2. Methodology
2.1. Preparation of peanut butter
A commercially available flowing-type, non-stabilized peanut butter
was used in all thermal inactivation experiments. Two-kilogram jars of
the product from the same production batch were purchased in order to
minimize variations in product composition and physicochemical
properties. Upon opening, the products were vigorously agitated for
10 min using a wire whisk in order to ensure thorough mixing. Aliquots
of 1.0 g were transferred into 4 cm × 6 cm Ziplock resealable poly-
ethylene pouches (0.15 mm thick, both sides). The peanut butter
medium in the plastic pouches were subjected to 15 KGy Gamma ir-
radiation in order to eliminate any background microflora that may be
present in the product or in the plastic pouch. This was performed in the
irradiation services facility of the Philippine Nuclear Research Institute
in Diliman, Quezon City, Philippines using a60Co package irradiator
(Comprad Communications, Hungary). After irradiation treatment, the
aerobic plate counts and mold and yeast counts were below the
2
LWT - Food Science and Technology 129 (2020) 109507
detection limit (< 1.0 log CFU/g) data not presented.
2.2. Physicochemical analyses and proximate composition determination
The peanut butter sample was subjected to physicochemical ana-
lyses and proximate composition determination following the methods
defined by the Association of Official Analytical Chemists (AOAC,
2012). Sample pH was determined following the electrometry method
(AOAC 981.12), while water activity was determined using a water
activity meter (Novasina, Pfaffikon, Switzerland) (AOAC 978.18). Fat
content was determined following the Soxhlet extraction technique
(AOAC 948.22b), while protein content was determined by employing
the Kjeldahl method (AOAC 950.48). The gravimetric methods were
employed in the determination of ash and moisture, following the
AOAC 950.49 and AOAC 925.40 protocols, respectively. Total carbo-
hydrates were determined by difference (Metzger & Nielsen, 2017). All
physicochemical and proximate composition analyses were conducted
in triplicate.
2.3. Microbial cultures
In this study, all tested organisms are maintained by the Laboratory
of Food Microbiology and Hygiene (LFMH), Department of Food
Science and Nutrition, College of Home Economics, University of the
Philippines Diliman. The test organisms included seven strains of S.
enterica, serovars Typhimurium (American Type Culture Collection,
ATCC 14028), Diarizonae (ATCC 12325 and ATCC 29934), Abortus-
Equi (ATCC 9842), Enteritidis (LFMH S1–10), Infantis (LFMH S2–10),
and Montevideo (LFMH S3–10). All LFMH bacterial strains were pre-
viously isolated from food and environment samples. Working cultures
were prepared by aseptically transferring stabs of each of the re-
frigerated stock cultures into separate 1 mL nutrient broth (NB,
HiMedia, India) and incubated at 35 °C for 18–24 h. Cells were obtained
from each of the culture and re-introduced to 1 mL NB for a 2nd culture
passage. Finally, loopfuls of cells from each of the 2nd passage cultures
were streaked onto nutrient agar (NA, HiMedia) slants and incubated
for another 18–24 h. The slant cultures were thereafter kept at a re-
frigerated temperature (4.0 °C) until used in the experiments.
2.4. Inoculum preparation, peanut butter inoculation, and pre-adaptation
Prior to inoculation to peanut butter, cells were propagated fol-
lowing the previously described 2-passage protocol. Cells in the sta-
tionary phase of the 2nd culture passage were used to prepare separate
inocula of each strain. Broth cultures were vortexed for 1 min to loosen
cell clumps. From each of the seven strains, 0.2-mL aliquots were
pooled in microcentrifuge tubes, which were spun on a benchtop cen-
trifuge (Cole Palmer, Illinois, USA) at 2400×g for 10 min. The super-
natant was decanted and the cell pellet was re-suspended in 1-mL
peanut oil by vortex-mixing under high speed for 5 min. The re-
suspended 7-strain cocktail of S. enterica was introduced into the peanut
butter sachets. The inoculated samples were re-sealed and massaged
manually for 1 min to ensure that the cells were evenly distributed in
the peanut butter emulsion. The samples were stored in sterile plastic
boxes and incubated at 35 °C for 24 h for pre-adaptation to the food
system prior to thermal inactivation.
2.5. Heat challenge study
The experiment set-up used in the thermal inactivation study is il-
lustrated in Fig. 1. With the use of binder clips, sealed plastic sachets
containing the inoculated samples were attached to a glass rod. The rod
was positioned in such a way that all peanut butter samples were
completely submerged (> 2.0 cm below water level) in a circulating
water bath (Lab Companion Batch Circulator, Jejo Tech, South Korea),
and allowed to equilibrate at the desired heating temperature (60, 65,
M.A.B. Pelaez, et al. LWT - Food Science and Technology 129 (2020) 109507

Table 1
Physicochemical properties and proximate composition of
flowing-type peanut butter.
Parametersa Values

pH 6.60 ± 0.02
aw 0.58 ± 0.00
Total fat 38.2 ± 2.00
Total protein 19.5 ± 0.30
Total carbohydrates 39.7 ± 4.00
Moisture 0.39 ± 0.02
Ash 2.20 ± 0.10

Fig. 1. Experiment set-up for the thermal inactivation studies of Salmonella
enterica in peanut butter. In all challenge temperatures, sachets containing in-
oculated peanut butter (PB) were suspended in a glass rod (GR) prior to being
immersed in hot water bath (WB). A thermometer (T) was inserted through the
cold point of an uninoculated sachet for temperature monitoring. Heat exposure
timing were started when the cold point reached the desired temperature.
a
Parameters are reported as averages ± SD of 3 values. pH
and aw were determined at 25.2 °C. Proximate components are
reported in g/100 g sample.
general linear model procedure (PROC GLM) of the SAS Statistical
Software Package version 8.0 (Cary, NC, USA). The Duncan's Multiple
Range Test was used for post-hoc determinations of significant differ-
ences at 95% level of significance.

70, 75, or 80 °C). For each inactivation run, one uninoculated peanut
3. Results and discussion
butter sample was used for temperature monitoring. This was done by
inserting a thermometer through the cold point of the sachet. When the
3.1. Physicochemical properties and proximate composition of test peanut
cold point temperature reached the desired experimental temperature,
butter
one sample is drawn out and transferred to an ice bath for not more
than 10 min. This sample was used in determining the initial population
The physicochemical properties and proximate composition of the
of S. enterica (population at t = 0). At pre-determined exposure inter-
peanut butter used as suspending medium in the heating studies are
vals, samples were sequentially taken out of the hot water bath and
summarized in Table 1. The pH value of 6.6 falls within the low acid
cooled as previously described. The samples were immediately sub-
range of food classification (Jay, 2000). On the other hand, this pro-
jected to serial 10- fold dilutions in 0.1% peptone water (PW, Hi-
duct's aw of 0.58 and the moisture content of 0.39 g/100 g sample
Media) and surface-plated onto NA plates (HiMedia). The contents of
makes the food product a low-moisture commodity (Jay, 2000). This aw
the sachets were transferred aseptically into screw-capped flasks con-
is slightly higher than those reported by previous researchers whose
taining 8 mL peptone water. Considering the paste-like consistency of
samples had aw < 0.4 (Burnett et al., 2000; He et al., 2011; Kataoka
the peanut butter sample, 1 mL of sterile peptone water was used to
et al., 2014). The total fat, protein, and carbohydrate contents of the
wash peanut butter adhering to the plastic by thorough massaging. The
test peanut butter are 38.2, 19.5, and 39.7 g/100 g, respectively. These
washing (slurry) was also collected into the flask in order to prepare the
are within the ranges reported by Li et al. (2014) for various com-
10-fold dilution. The flask was then vigorously agitated by vortexing at
mercially available peanut butter and peanut butter spreads including
high speed for 5 min. The resulting slurry was further subjected to serial
omega-3 fatty acid-enriched, regular, reduced sugar, and reduced fat
10-fold dilutions with PW. Aliquots of 0.1 mL were withdrawn from
samples.
appropriate dilutions and surface-plated in non-selective NA plates and
incubated at 35 °C for 24 h before survivor enumerations, as similarly
done by Ma et al. (2009). 3.2. Thermal inactivation of S. enterica in flowing-type peanut butter

Survival curves of S. enterica heated in flowing-type local peanut

2.6. Determination of inactivation parameters
butter at 60, 65, 70, 75, and 80 °C are presented in Fig. 2a–e. During the
come-up time (time to reach the treatment temperature, t = 0), the
All survivor populations of test organisms were expressed as log
Salmonella counts were reduced by 0.1–0.3 log CFU/g (data not pre-
CFU/g. The death kinetic parameters were determined using linear
sented). When Salmonella in peanut butter was heated at 60 and 65 °C
regression. Inactivation curves were generated using the freeware
for 60 min, only 1.38- and 1.25-log CFU/g reductions, respectively,
Excel® add-in DMFit 3.0 (Institute of Food Research, Reading
were observed. As treatment temperature was increased, the rate of
Laboratory, UK). The decimal reduction time (DT value) was de-
Salmonella inactivation also increased, with total reductions of, 2.10,
termined by obtaining the negative inverse of the slope of the survival
2.58, and 3.07 log CFU/g at 70, 75, and 80 °C respectively, within
curve. The DT value measures the resistance of the test organism to an
60 min. The cocktail of S. enterica generally exhibited a monophasic,
inactivating agent and is defined as the unit time of exposure of the cells
logarithmic linear inactivation curve in the heated peanut butter
to a heating temperature that shall result in 1 log reduction (90%) in
medium with R2 values > 0.90. This inactivation behavior was simi-
the initial population (Jay, 2000). The thermal resistance constant (z
larly described by Moats (1971) for organisms in heated food matrices,
value) was also determined and is equivalent to the increase in the
and is a hallmark of a first-order death kinetics. When the first-order
heating temperature needed to reduce the DT value by 10-fold, or in-
death kinetic approach was used by Ma et al. (2009), they also observed
crease the process lethality by 10-fold. The z-value was determined by
linear inactivation behavior in three groups of S. enterica in peanut
obtaining the negative inverse of the slope of the regression line of the
butter heated to 77, 81, 83, and 90 °C. The reported R2 values ranged
log of DT values against temperatures (Jay, 2000).
from 0.85 to 0.98 for S. Tennessee outbreak isolates, 0.95 to 0.97 for S.
Tennessee sporadic case isolates, and 0.89 to 0.98 for mix of other
2.7. Statistical analysis strains including S. Enteritidis, Typhimurium, and Heidelberg. A 5-
strain cocktail of S. enterica also exhibited similar inactivation pattern
Data obtained from independently replicated experiments were in different peanut butter samples heated to 72 and 90 °C (He et al.,
subjected to single-factor analysis of variance (ANOVA) using the 2011). A log-linear inactivation behavior was similarly observed by

3
M.A.B. Pelaez, et al. LWT - Food Science and Technology 129 (2020) 109507

Fig. 2. Thermal inactivation curves of Salmonella enterica in Philippine flowing-type peanut butter heated to (a.) 60, (b.) 65, (c.) 70, (d.) 75, and (e.) 80 °C from which
the decimal reduction times (D-values) were determined. The plots were generated from averages of survivor populations obtained from 2 independent experimental
runs, with 2 internal replicates per run. The thermal resistance parameter, z-value, was similarly determined by plotting the log of D-value vs. heating temperature
(f.).

Wright et al. (2017) for a multi-strain cocktail of S. enterica in peanut resistance of S. enterica by 58% (3.75 min) to 68% (4.91 min) (He et al.,
butter heated to > 90 °C. 2011).
It is difficult to compare the results of this current work with pre-
vious studies due to variations in implicit microbial characteristics,
3.3. DT- and z-values
intrinsic food properties, and extrinsic process variables employed in
the experiments. However, what is apparent from the results of this
The DT values calculated from the negative inverse of the slope of
work and those that were previously published is the very high thermal
the log-linear inactivation curves fitted in each heating temperature are
resistance of S. enterica in peanut butter. In this study, although a
shown in Table 2. As expected, the thermal resistance of S. enterica
general decrease in DT values were observed as the heating temperature
decreased with increasing heating temperature. A 10-degree increase
increased, the D60, D65, and D70, were found to be not significantly
from 60° to 70 °C in the heating temperature only resulted in 35%
different (p > 0.05) from each other. It was only when the tempera-
difference (16.75 min) in the DT value of the test organism. When the
ture was increased to at least 75 °C that a significant decrease
heating temperature was increased from 70 to 80 °C, a difference of
(p < 0.05) in the thermal resistance of S. enterica was observed, which
48% (15.08 min) in the thermal resistance was observed. This value
almost halved that the thermal resistance of the organism at the lowest
was comparable to those reported by Ma et al. (2009) for 3 separate
tested heating temperature. Further increase of challenge temperature
cocktails of S. enterica challenged in peanut butter who reported a
to 80 °C resulted in a 3-fold reduction of thermal resistance at 60 °C.
change in thermal resistance of 37% (9.8 min) to 45% (13.3 min) when
Not surprisingly, the thermal resistance constant (z-value, Fig. 2f) of
the heating temperature was increased from 71 to 83 °C. On the con-
the cocktail of S. enterica challenged in this study was also high at
trary, in this current study, increasing the heating temperature from 60
44.5 °C (Table 2). This means that within the range tested in this study,
to 80° resulted in 66% (31.83 min) difference in the thermal resistance
an increase in the heating process temperature by this much will reduce
of the challenge organisms; which was lower than those reported by Ma
the DT value by 10 folds. Despite the differences in variables employed
et al. (2009) who observed 54–69% change in thermal resistance when
in the experiments, this z-value is within the range reported by Ma et al.
the heating temperature was increased from 71 to 90 °C. In an ex-
(2009), which was 38.97–55.9 °C. The high thermal resistance of S.
perimental design similar to that applied in this study, a change of
enterica in peanut butter may be attributed to the thermal cross-pro-
heating temperature from 72 to 90 °C resulted in changes in the thermal
tection rendered by pre-conditioning in low water activity environ-
ments. In the study of He et al. (2011), which similarly involved a
Table 2
Thermal inactivation kinetic parametersa of S. enterica in flowing-type peanut
cocktail of S. enterica in different peanut butter suspending media,
butter. longer exposure to the peanut butter menstruum prior to the thermal
challenge studies increased the thermal resistance of the cells at 72 and
Heating Temperatures (°C) DT-values (min) z-value (°C)
90 °C.
60 47.98 ± 2.15a 44.50 ± 5.14
65 40.07 ± 5.25ab
70 31.23 ± 5.88abc 4. Conclusion and recommendations
75 25.54 ± 2.93bc
80 16.15 ± 4.05c
Results of this study demonstrate that S. enterica exhibited high
abc
Values on the same column followed by the same letters are not significantly resistance in flowing-type peanut butter medium subject to heat treat-
different (p > 0.05). ment between 60 and 80 °C. Despite the microbiological stability of
a
Parameters are reported as averages ± SD of 4 values obtained from 2 low-moisture food such as peanut butter, results of this study showed
independent runs. that it requires a relatively severe thermal process if safety against

4
M.A.B. Pelaez, et al.
pathogenic microorganisms such as S. enterica is to be achieved. This is
particularly important among micro- and small-scale local processors of
peanut butter whose food safety programs are not well-established and
cross-contamination risks during processing are significant.
Consequently, these results underscore the importance of employing
Good Manufacturing and Hygienic Practices in the process flow of such
commodity. The efficacy of other pathogen-reducing hurdles, in com-
bination with thermal processing should be considered.
CRediT authorship contribution statement
Mark Anthony B. Pelaez: Conceptualization, Methodology, Formal
analysis, Writing - original draft. Gerieka R. Anapi: Formal analysis,
Writing - original draft. Donna V. Bautista: Formal analysis, Writing -
original draft. Ma. Dulce P. Dallo: Formal analysis, Writing - original
draft. Joseph Conrad M. Libunao: Formal analysis, Writing - original
draft. Alonzo A. Gabriel: Conceptualization, Methodology, Formal
analysis, Writing - original draft.
Declaration of competing interest
The authors whose names are listed above certify that they have no
affiliations and relationships with any organization or entity with any
financial interest or non-financial interest in the subject matter or
materials discussed in this manuscript.
Acknowledgements
This study was made possible by the Outright Research Grant of the
University of the Philippines Diliman Office of the Vice Chancellor for
Research and Development (Project Number 202013 ORG). This work
was also partially supported by the Philippine Council for Industry,
Energy and Emerging Technology Research and Development,
Department of Science and Technology (DOST), through its Human
Resource Development Program (HRDP).
References
Association of Official Analytical Chemists (Aoac) International (2012). In (19th ed.). G.
W. Latimer (Vol. Ed.), Official methods of analysis of AOAC international: Vol. 2.
Gaithersburg, MD, USA: AOAC International.
Burnett, S. L., Gehm, E. R., Weissinger, W. R., & Beuchat, L. R. (2000). Survival of
Salmonella in peanut butter and peanut butter spread. Journal of Applied Microbiology,
89, 472–477.
Centers for Disease Control and Prevention, Cdc. (2007). Multistate outbreak of
Salmonella Tennessee infections linked to peanut butter (FINAL UPDATE). Available
from: https://www.cdc.gov/salmonella/2007/peanut-butter-3-7-2007.html.
Centers for Disease Control and Prevention, Cdc. (2009). Multistate outbreak of
Salmonella Typhimurium infections linked to peanut butter, 2008-2009 (FINAL
UPDATE). Available from: https://www.cdc.gov/salmonella/2009/peanut-butter-
2008-2009.html.
Centers for Disease Control and Prevention, Cdc. (2012). Multistate outbreak of
Salmonella bredeney infections linked to peanut butter manufactured by sunland, Inc.
(final update). Available from: https://www.cdc.gov/salmonella/bredeney-09-12/
index.html.
Centers for Disease Control and Prevention, Cdc. (2013). Notes from the field: Salmonella
bredeney infections linked to a brand of peanut butter — United States, 2012.
Available from: https://www.cdc.gov/mmwr/preview/mmwrhtml/mm6206a4.htm.
Deng, X., Li, Z., & Zhang, W. (2012). Transcriptome sequencing of Salmonella enterica
serovar Enteritidis under desiccation and starvation stress in peanut oil. Food
Microbiology, 30, 311–315.
Finn, S., Condell, O., McClure, P., Amézquita, A., & Fanning, S. (2013). Mechanisms of
LWT - Food Science and Technology 129 (2020) 109507
survival, responses and sources of Salmonella in low-moisture environments. Frontiers
in Microbiology, 4–331, 1–15.
Fong, K., & Wang, S. (2016). Heat resistance of Salmonella enterica is increased by pre-
adaptation to peanut oil or sub-lethal heat exposure. Food Microbiology, 58, 139–147.
Galvez, F. C., Francisco, M. L., Lustre, A. O., & Resurreccion, A. V. A. (2006). Quality
improvement for local unstabilized peanut butter. United States agency for international
development peanut collaborative Research support program project 04 monograph series
No. 6.
Gruzdev, N., Pinto, R., & Sela, S. (2011). Effect of desiccation on tolerance of Salmonella
enterica to Multiple stresses. Applied and Environmental Microbiology, 77, 1667–1673.
He, Y., Guo, D., Yang, J., Tortorello, M. L., & Zhang, W. (2011). Survival and heat re-
sistance of Salmonella enterica and Escherichia coli O157:H7 in peanut butter. Applied
and Environmental Microbiology, 77, 8434–8438.
Herriman, R. (2014). Philippines FDA: Arrowhead Mills peanut butter recalled due to
Salmonella risk. Available from: http://outbreaknewstoday.com/philippines-fda-
arrowhead-mills-peanut-butter-recalled-due-to-salmonella-risk-49470/.
Jay, J. M. (2000). High-temperature food preservation and characteristics of thermophilic
microorganisms. Modern food Microbiology (pp. 341–362). Boston, MA: Springer US.
Kataoka, A., Enache, E., Black, D. G., Elliott, P. H., Napier, C. D., Podolak, R., et al.
(2014). Survival of Salmonella Tennessee, Salmonella Typhimurium DT104, and
Enterococcus faecium in peanut paste formulations at two different levels of water
activity and fat. Journal of Food Protection, 77, 1252–1259.
Keller, S. E., Grasso, E. M., Halik, L. A., Fleischman, G. J., Chirtel, S. J., & Grove, S. F.
(2012). Effect of Growth on the Thermal Resistance and Survival of Salmonella
Tennessee and Oranienburg in peanut butter, measured by a new thin-layer thermal
death time device. Journal of Food Protection, 75, 1125–1130.
Kilonzo-Nthenge, A., Rotich, E., Godwin, S., & Huang, T. (2009). Consumer storage period
and temperature for peanut butter and their effects on survival of Salmonella and
Escherichia coli O157:H7. Food Protection Trends, 29, 787–792.
Li, C., Huang, L., & Chen, J. (2014). Comparative study of thermal inactivation kinetics of
Salmonella spp. in peanut butter spread. Food Control, 45, 143–149.
Mattick, K. L., Jørgensen, F., Wang, P., Pound, J., Vandeven, M. H., Ward, L. R., et al.
(2001). Effect of challenge temperature and solute type on heat tolerance of
Salmonella serovars at low water activity. Applied and Environmental Microbiology, 67,
4128–4136.
Ma, L., Zhang, G., Gerner-Smidt, P., Mantripagada, V., Ezeoke, I., & Doyle, M. (2009).
Thermal inactivation of Salmonella in peanut butter. Journal of Food Protection, 72,
1596–1601.
Merueñas, M. (2009). 2 more batches of peanut butter products positive for Salmonella –
report. Available from: http://www.gmanetwork.com/news/news/nation/153860/
2-more-batches-of-peanut-butter-products-positive-for-salmonella-report/story/.
Metzger, L. E., & Nielsen, S. S. (2017). Nutrition labeling. In S. S. Nielsen (Ed.). Food
analysis (pp. 35–44). (5th ed.). Switzerland: Springer International Publishing AG.
Moats, W. A. (1971). Kinetics of thermal death of bacteria. Journal of Bacteriology, 105,
165–171.
Podolak, R., Enache, E., Stone, W., Black, D. G., & Elliott, P. H. (2010). Sources and risk
factors for contamination, survival, persistence, and heat resistance of Salmonella in
low-moisture foods. Journal of Food Protection, 73, 1919–1936.
Sánchez-Maldonado, A. F., Lee, A., & Farber, J. M. (2018). Methods for the control of
foodborne pathogens in low-moisture foods. Annu. Rev. Food Sci. Technol. 9, 177–208.
Shachar, D., & Yaron, S. (2006). Heat tolerance of Salmonella enterica serovars Agona,
Enteritidis, and Typhimurium in peanut butter. Journal of Food Protection, 69,
2687–2691.
Sheth, A. N., Hoekstra, M., Patel, N., Ewald, G., Lord, C., Clarke, C., et al. (2011). A
national outbreak of Salmonella serotype Tennessee infections from contaminated
peanut butter: A new food vehicle for salmonellosis in the United States. Clinical
Infectious Diseases, 53, 356–362.
Song, W.-J., & Kang, D.-H. (2016). Influence of water activity on inactivation of
Escherichia coli O157:H7, Salmonella Typhimurium and Listeria monocytogenes in
peanut butter by microwave heating. Food Microbiology, 60, 104–111.
United States Department of Agriculture (Usda) (2018). PP16 USDA commodity re-
quirements: Peanut products for use in domestic programs. Available from: https://
www.ams.usda.gov/sites/default/files/media/PP16CommodityRequirements.pdf.
United States Environment Protection Agency (Usepa) (2009). Peanut processing.
Available from: https://www3.epa.gov/ttn/chief/ap42/ch09/final/c9s10-2b.pdf.
U.S. Food and Drug Administration (Usfda). (2012). Inspection report: FEI number
1000117188. Available from: http://www.fda.gov/downloads/AboutFDA/
CentersOffices/OfficeofGlobalRegulatorOperationsandPolicy/ORA/
ORAElectronicReadingRoom/UCM324793.pdf.
Woodroof, J. G. (1983). Peanuts: Production, processing, products (3rd ed.). Westport CT:
AVI Publishing Company, Inc.
Wright, D. G., Minarsich, J., Daeschel, M. A., & Waite-Cusic, J. (2017). Thermal in-
activation of Salmonella spp. in commercial tree nut and peanut butters in finished
packaging. Journal of Food Safety, e12371, 1–6.