Food Microbiology 92 (2020) 103571

Contents lists available at ScienceDirect

Food Microbiology
journal homepage: www.elsevier.com/locate/fm

Microbial safety of oily, low water activity food products: A review T

a,∗∗ b,c,∗ a c
Amin N. Olaimat , Tareq M. Osaili , Murad A. Al-Holy , Anas A. Al-Nabulsi ,
Reyad S. Obaidb, Akram R. Alaboudid, Mutamed Ayyashe, Richard Holleyf
a
Department of Clinical Nutrition and Dietetics, Faculty of Applied Medical Sciences, The Hashemite University, P.O. Box 150459, Zarqa, 13115, Jordan
b
Department of Clinical Nutrition and Dietetics, College of Health Science, University of Sharjah, Sharjah, United Arab Emirates
c
Department of Nutrition and Food Technology, Jordan University of Science and Technology, P.O. Box 3030, Irbid, 22110, Jordan
d
Department of Pathology and Public Health, Faculty of Veterinary Medicine, Jordan University of Science and Technology, P.O. Box 3030, Irbid, 22110, Jordan
e
Department of Food, Nutrition and Health, College of Food and Agriculture, United Arab Emirates University (UAEU), Al Ain, UAE
f
Department of Food Science and Human Nutrition, University of Manitoba, Winnipeg, Manitoba, R2J 3L8, Canada

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

Keywords: Oily, low water activity (OL aw) products including tahini (sesame seed paste), halva (tahini halva), peanut
Low water activity butter, and chocolate, have been recently linked to numerous foodborne illness outbreaks and recalls. This
Oily foods review discusses the ingredients used and processing of OL aw products with a view to provide greater under-
Tahini standing of the routes of their contamination with foodborne pathogens and factors influencing pathogen per-
Halva
sistence in these foods. Adequate heat treatment during processing may eliminate bacterial pathogens from OL
Peanut butter
Chocolate
aw foods; however, post-processing contamination commonly occurs. Once these products are contaminated,
their high fat and sugar content can enhance pathogen survival for long periods. The physiological basis and
survival mechanisms used by pathogens in these products are comprehensively discussed here. Foodborne
outbreaks and recalls linked to OL aw foods are summarized and it was observed that serotypes of Salmonella
enterica were the predominant pathogens causing illnesses. Further, intervention strategies available to control
foodborne pathogens such as thermal inactivation, use of natural antimicrobials, irradiation and hydrostatic
pressure are assessed for their usefulness to achieve pathogen control and enhance the safety of OL aw foods.
Sanitation, hygienic design of manufacturing facilities, good hygienic practices, and environmental monitoring
of OL aw food industries were also discussed.

1. Fatty or oily, low water activity (OL aw) foods
Foods with low water activity (aw) (< 0.70) have a long shelf life
and can be shelf stable for years. The number of food items and food
ingredients considered to be or that can contribute to the low aw of a
food are almost limitless. Examples of products in this category include
soup mixes, spices, herbs, nuts, dried fruits and vegetables, dried meats,
chocolate, cocoa, pasta, breakfast cereals, cake mixes, powdered milk
and infant formula, egg powder, hydrolyzed vegetable protein, snacks,
peanut butter, honey, jams, grains, seeds, tahini and halva (Beuchat
et al., 2013, 2012; Blessington et al., 2013).
The interaction of low aw products with foodborne pathogens was
previously discussed in several review articles (Beuchat et al., 2013;
Grocery Manufacturers Association, GMA, 2009). Additional papers
related to this subject have been published after these reviews. This
review focuses on low aw foods that are high in oil, particularly tahini
(sesame paste), halva (tahini halva), peanut butter, and chocolate.
These products contain an unusually high amount of fat and low levels
of water and thus have low aw which may protect the pathogens from
the heat treatment during processing or other post-processing inter-
ventions. Tahini contains 58% fat, 0.04% water and has an aw of 0.18
(Osaili et al., 2016). Halva contains 35.6% fat, 1.64% water and also
has an aw of 0.18 (Osaili et al., 2018b). Peanut butter contains 55% fat,
0.5–2% water and has an aw of 0.20–0.33 (Burnett et al., 2000), while
chocolate contains 30% fat and has an aw of 0.4–0.5 (Lake et al., 2010).
These products have an extended shelf life of 1–2 years at room tem-
perature and they are used as ready-to-eat (RTE) products or as in-
gredients in other products.
These products for long time were considered to be micro-
biologically safe because of their low aw level and high fat and sugar
contents. Nevertheless, recently, they have been shown to be con-
taminated with pathogenic microorganisms, commonly Salmonella spp.,

∗
Corresponding author. Department of Clinical Nutrition and Dietetics, College of Health Science, University of Sharjah, Sharjah, United Arab Emirates.
∗∗
Corresponding author.
E-mail addresses: aminolaimat@hu.edu.jo (A.N. Olaimat), tosaili@just.edu.jo, tosaili@sharjah.ac.ae (T.M. Osaili).

https://doi.org/10.1016/j.fm.2020.103571
Received 25 February 2020; Received in revised form 17 May 2020; Accepted 13 June 2020
Available online 21 June 2020
0740-0020/ © 2020 Elsevier Ltd. All rights reserved.
A.N. Olaimat, et al. Food Microbiology 92 (2020) 103571

Fig. 2. Halva production (UNIDO, 2003)* Control measure (time/temperature

control or cleaning and sanitation procedures) can be applied to reduce the risk
of foodborne pathogens.

leading to several foodborne illness outbreaks and food product recalls.

The objectives of this review are to discuss the steps used to process
oily, low aw (OL aw) foods (tahini, halva, peanut butter, chocolate), to
collect the scattered data about the prevalence of foodborne pathogens
in these products, to summarize the illness outbreaks and recalls linked
to these foods, to investigate the survival potential of pathogens in these
products and characterize the mechanisms used to enable their survival
and discuss the strategies that could be used to control them in these
products.

2. Processing of OL aw foods

2.1. Manufacture of tahini and halva

Tahini and halva-making technologies are based on traditional

Fig. 1. Tahini production (UNIDO, 2003) * Control measure (time/temperature
control or cleaning and sanitation procedures) can be applied to reduce the risk
of foodborne pathogens.
methods and have been described in the literature in detail (QUALEB,
2015; Mureşan et al., 2013). The technological features of tahini and
halva manufacture are presented schematically in Figs. 1 and 2, re-
spectively.
Tahini is mainly manufactured by milling roasted and dehulled se-
same seeds (QUALEB, 2015). The first stage of the process involves
washing and drying sesame seeds using special machines to remove the

2
A.N. Olaimat, et al. Food Microbiology 92 (2020) 103571

sand and other foreign material. Some studies describe the use of dif-
ferent seeds such as those from the sunflower to produce sunflower
tahini (Damir, 1984), or sunflower butter (González-Pérez and
Vereijken, 2007; Lima and Guraya, 2006). After washing, dried sesame
seeds are dehulled and roasted, and these steps represent the basic and
most important operations in tahini and halva manufacturing that af-
fect the quality of these products. Dehulling improves the color of tahini
and masks the bitter taste by removing most of the oxalic acid and fiber
found in the seed coats (Elleuch et al., 2014; Ereifej et al., 2005).
Roasting of sesame seeds promotes the desired texture, color and flavor
of the finished product (Akbulut and Oklar, 2008; Kahyaoglu and Kaya,
2006; Zahedi and Mazaheri-Tehrani, 2012), and inactivates pathogenic
organisms (Torlak et al., 2013). Once roasted, the seeds are ground,
mixed, cooled and filled in plastic bottles (QUALEB, 2015).
Halva is produced by mixing tahini paste with water, sugars, acid,
soapwort root extract and emulsifying agents (Sanja et al., 2015).
Soapwort extract is a natural additive, produced by boiling soapwort
roots in water (Shakerardekani and Shahedi, 2015). The active in-
gredients, saponins, are found in many plant foods such as soybeans,
chick peas, as well as peanuts (Güçlü-Üstündağ and Mazza , 2007) and
is used in halva for color, to improve volume plus texture and to prevent
the separation of sesame oil from halva (Çam and Topuz, 2018; Turkish
Food Codex, 2004).
Other approved food ingredients and chemical agents are used to
improve the physiochemical properties of halva such as vanilla, cho-
colate, nuts, palm oil, honey, date syrup, molasses, egg white, soy
protein extract, and the whitening agent, titanium dioxide (Çiftçi et al.,
2008; Elleuch et al., 2014; Guneser and Zorba, 2014), and the finished
product is filled in plastic bottles.

2.2. Manufacture of peanut butter

Peanut butter manufacture based on conventional methods has been

described in detail recently (CFR, 2018) and technological features of
the process are summarized in Fig. 3. After the peanuts arrive at the
plant, processing begins by removing foreign material from the peanut
pods using special sieves and blowers (Woodroof, 1983). The outer shell
of the cleaned peanuts is removed by passing pods between rollers and
the shelled peanuts are used as the starting materials for peanut butter
production (Aryana et al., 2003; Sanders et al., 2014). Roasting is the
most critical step for controlling the quality of the final products
(Woodroof, 1983). The shelled nuts are treated in the roaster at
160–180 °C for 40–60 min (Arya et al., 2016). Roasting temperature
and time differ with the specific characteristics required for the finished Fig. 3. Schematic arrangement of peanut butter stages (Mohd Rozalli, 2015)*
product like color or moisture content (Sanders et al., 2014). Control measure (time/temperature control or cleaning and sanitation proce-
Cooling the roasted peanuts takes place through the use of air dures) can be applied to reduce the risk of foodborne pathogens.
blowers and heat exchangers to stop the development of undesirable
browning and unpleasant flavors due to retained heat. Different
manufacture are shown in Fig. 4. Fresh cocoa beans are dried and
blanching processes comprising dry, water, spinning, and air impact are
fermented to develop flavor and desired color (Fowler, 2009). Drying
used to treat the cooled, roasted peanuts. The dry blanching process is
plays a major role in flavor development during chocolate making. The
preferred because it helps remove the skin of the nuts and the heart
moisture level of fermented beans needs to be 7–8%; if it is below, the
kernels (Sanders et al., 2014). Dry blanching involves heating the nuts
beans will very likely become brittle and difficult to process, and if it is
to 138–140 °C for 20–25 min to control the moisture content of the
above, they become moldy (Beckett, 2009). Fermented cocoa beans are
finished product at about 1.2%. Finally, the blanched/roasted nuts are
cleaned by passage through graded sieves to remove all the unnecessary
mechanically ground into a paste using one of several grinding methods
materials surrounding the beans. The beans are roasted to develop the
(Mohd Rozalli, 2015). In addition, other ingredients are added to the
flavor and texture of chocolate (Giacometti et al., 2015). The normal
paste such as vegetable fats, salt, seasoning and flavoring agents (CFR,
roasting temperature is between 110 and 140 °C for 45 min to 1 h
2018). During grinding, the temperature can rise up to 60 °C and, to-
(Beckett, 2009). After roasting, the shells of the beans are broken in a
gether with entrapped air bubbles, may cause oxidation (APV an SPX
cracker. Winnowing will separate valuable product (cocoa nibs) from
brand, 2008). Cooling the mix and preventing air incorporation im-
the shell of the beans. After that, coca nibs are milled to change them
prove the keeping quality of the finished product (CFR, 2010). The
into a chocolate liquid (Asep et al., 2008). Sugar, milk powders and
paste, peanut butter, is vacuum filled into glass or plastic jars.
sweetened condensed milk are usually used in the production of cho-
colate. The size of particles in the mixed ingredients is reduced by
2.3. Manufacture of chocolate confectionery
different refiners. This process consists of three or five metal rollers
with distance adjustable between the latter and the sticky mass of
The schematic manufacturing steps of chocolate confectionery

3
A.N. Olaimat, et al.
Fig. 4. Schematic manufacturing steps of chocolate confectionery (Beckett,
2009)* Control measure (time/temperature control or cleaning and sanitation
procedures) can be applied to reduce the risk of foodborne pathogens.
mixed ingredients (Winkler, 2014).
Conching and tempering are important steps for flavor and texture
development of chocolate. The dairy ingredients and sugar plus the
4
Food Microbiology 92 (2020) 103571
refined powder mass are mixed for several hours at 50–90 °C.
Temperature mainly depends on the kind of chocolate produced
(Winkler, 2014). The smooth liquid chocolate is cooled to 29–31 °C to
solidify the mass and stored at defined temperatures and humidity
(Winkler, 2014).
3. Contamination of OL aw foods with foodborne pathogens
The contamination of OL aw products foods with foodborne patho-
gens may occur during growth, storage or processing (Podolak et al.,
2010; Sheth et al., 2011). Pathogens which were isolated from the
major raw component (eg. cacao beans, sesame seeds and peanuts) of
OL aw foods have also been found at the processing stage of the food
chain which means that these pathogens may originate from the pro-
duction environment and survive until processing (Frank, 2014). Pa-
thogenic bacteria may contaminate cacao beans, nuts and sesame seeds
in the crops during production from different sources including the soil,
contaminated irrigation water, air, plant microflora, fertilizers, recon-
stituted insecticides and fungicides, birds, dust, rodents, insects, live-
stock, and human handling (Olaimat and Holley, 2012). Additional
bacterial contamination potentially may occur during post-harvest
processing due to poor sanitation of harvesting and processing equip-
ment, transport containers and vehicles, rinse water, ice, and human
handling (Olaimat and Holley, 2012). Sesame seed contamination,
particularly with Salmonella, may occur during cultivation (soil,
manure, water, birds), storage (poor sanitation) and after heat treat-
ment (Pui et al., 2011). Willis et al. (2009) found that the prevalence of
Salmonella in sesame seed samples in the UK was 1.7% (13/771). In
another study, Salmonella was isolated from 11.3% (20/177 of samples
collected between 2006 and 2009) and 9.9% (23/233 of samples col-
lected in 2010) of imported sesame seed in the US (Van Doren et al.,
2013a, 2013b). Nascimento et al. (2018) analyzed 414 samples of
peanuts and peanut products taken throughout the peanut supply chain
in Brazil (129 samples from post-harvest, 185 samples from secondary
processing and 100 samples from the retail market) for the presence of
Salmonella, Escherichia coli and Enterobacteriaceae. They detected high
Enterobacteriaceae numbers in the post-harvest samples and 16% of the
samples remained contaminated at the end of the secondary processing.
E. coli was detected in 7 (1.7%) samples (6 samples from primary
production and 1 peanut butter sample), while Salmonella was isolated
from 9 (2.2%) samples (6 from post-harvest samples, 2 from the initial
stage of the secondary processing samples and 1 from the retail sam-
ples). On the other hand, Zhang et al. (2017) did not detect Salmonella
in 279 sesame seed samples at retail establishments in the US. Con-
tamination of OL aw food products with foodborne pathogens during
processing and post-processing storage is primarily due to cross-con-
tamination (Carrasco et al., 2012; Podolak et al., 2010). It has been
reported that processed low aw foods (given a treatment consisting
mainly of heat to inactivate foodborne pathogens) were responsible for
63% of worldwide foodborne illness outbreaks caused by low aw foods
and 54% of US recalls associated with low aw foods between 2007 and
2012. On the other hand, minimally processed low aw foods which were
not given a lethal step were associated with only 12% of worldwide
outbreaks and 35% of US recalls (Frank, 2014). It seems that processed
products which receive more treatments, have higher potential risk of
contamination from the processing environment. However, when the
standard guidelines are applied in processing of chocolate, peanut
butter and tahini, raw cocoa beans, sesame seed and nuts are exposed to
roasting heat treatment (110–140 °C) which inhibit foodborne patho-
gens before packaging. Therefore, the lack of adequate heat process
could be the major source of pathogen contamination since the pre-
processing contaminating pathogens will remain and survive during the
insufficient heat treatment (Frank, 2014; Podolak et al., 2010) and
there is no subsequent chocolate manufacturing step able to eradicate
Salmonella from these products (Bean and Post, 2014). For example,
insufficient heat treatment of peanuts during roasting was the major
 A.N. Olaimat, et al.

Table 1
Salmonellosis outbreaks associated with the consumption of peanut butter, chocolate, tahini and halva.
Product Product source S. enterica serovar Year Number of cases Isolated from product? Outbreak location(s) Source

Peanut butter Australia S. Mbandaka 1996 15 yes Australia CDC, 2007a, 2007b; Scheil et al. (1998); Sheth
et al. (2011)
Peanut butter USA S. Tennessee 2006–07 715 yes USA (48 states)
Peanut butter, peanut butter– USA S. Typhimurium 2008–09 714 yes USA (46 states), one case in Canada Cavallaro et al. (2011); CDC, 2009,2010
containing products
Peanut butter USA S. Bredeney 2012 42 no USA (20 states) CDC, 2012a, 2013a
Peanut butter and/or almond butter S. Braenderup 2014 6 no (yes from environment USA (5 states) CDC, 2014
samples)
Halva Turkey S. Typhimurium DT 104 2001 27 (Sweden) yes Australia, Germany, Norway, Sweden, Aavitsland et al. (2001); Brockmann (2001); de
18 (Norway) United Kingdom Jong et al. (2001); Little (2001);
17 (Australia) O’Grady et al. (2001)
Tahini Egypt S. Montevideo 2002 55 yes Australia Tauxe et al. (2008); Unicomb et al. (2005)
Tahini Lebanon S. Montevideo 2003 3 yes Australia Unicomb et al. (2005)

5
Tahini and halva Lebanon S. Montevideo 2003 10 yes New Zealand Unicomb et al. (2005)
Tahini and hummus Lebanon S. Bovismorbificans 2011 23 yes USA (7 states) CDC, 2012b
Tahini and hummus Turkey S. Montevideo 2012 12 yes New Zealand NZPHS, 2013; Paine et al. (2014)
S. Mbandaka 3
S. Maastricht 1
Tahini Turkey S. Montevideo, 2013 16 yes USA (9 states) CDC, 2013b
S. Mbandaka
Sesame-based food products (incl. Salmonella enterica 2016– 40 yes EU Member States (Greece, Germany, ECDC, 2017
tahini and seeds) 11:z41:enz15 (new serotype) 2017 Czech Republic, Luxembourg)
Tahini Israel S. Concord 2018 8 yes USA (4 states) FDA, 2018
Tahini USA S. Concord 2019 6 yes USA (3 states) CDC, 2019
Chocolate Italy S. Napoli 1982 245 yes UK Gill et al. (1983)
Chocolate Norway S. Typhimurium 1987 361 yes Norway, Finland Kapperud et al. (1990)
Chocolate Germany S. Oranienburg 2001–02 459 yes Germany Werber et al. (2005)
Chocolate UK S. Montevideo 2006 40 yes UK Vasager (2006)

Adapted from Harris et al. (2019).

Food Microbiology 92 (2020) 103571
A.N. Olaimat, et al.
reason for S. Typhimurium persistence in peanuts and peanut butter
which led to a multistate illness outbreak involving 714 persons in the
US during 2008–2009 (Cavallaro et al., 2011). A high occurrence of E.
coli (100% and 89% positive) has been found during cocoa bean drying
and storage before initiation of processing. While after roasting, only
one sample out of 119 cocoa bean samples was positive for Salmonella
(Nascimento et al., 2010). Several large outbreaks of salmonellosis have
occurred in Europe, Canada and the US due to the consumption of
chocolate contaminated with Salmonella which was isolated from the
implicated chocolate many months after the outbreaks. It has been re-
ported that the use of heating at 105 °C for few seconds in chocolate
reduces Salmonella numbers by only 1 log CFU/g (Beuchat et al., 2013).
The first salmonellosis outbreak linked to chocolate in the US occurred
in 1973 and included 119 illnesses. This outbreak was linked to con-
taminated raw cocoa beans where Salmonella was isolated from the dust
at the bean processing areas which may also have contaminated the
final product (Craven et al., 1975).
A number of foodborne pathogens have been isolated from OL aw
food products; however, Salmonella is the pathogen of most concern
linked to several recalls and illness outbreaks associated with OL aw
foods. For example, Salmonella was associated with 94% of recalls in the
US and 53% of total worldwide outbreaks associated with low aw
products between 2007 and 2012. Ayaz et al. (1986) found that two of
10 tahini plants (20%) in Saudi Arabia were positive for Salmonella and
4 serotypes (S. Hadar, S. Agona, S. Einsbuettel and S. Ubrecht) were
isolated. Özkaya (1988) reported that 1% (1/93) of halva samples in
Turkey were positive for Salmonella. Brockmann et al. (2004) isolated
Salmonella from 8% (1/12) of tahini, 11% (8/71) of halva and 13% (2/
16) of sesame seeds in Germany. Alaouie et al. (2017) isolated Salmo-
nella and generic E. coli from 17% (7/42) and 43% (18/42), respec-
tively, from tahini produced in Lebanon. Gokmen et al. (2016) also
isolated Salmonella from 6.6% (1/15) of halva samples in Balıkesir in
Turkey. However, Yamani and Isa (2006) found that the 42 tahini
samples collected from 14 manufacturing plants in Jordan were free of
Salmonella. Kahraman et al. (2010) and Sengun et al. (2005) also re-
ported that Salmonella was not detected in 120 (from Marmara) and 63
(from Izmir) halva samples, respectively, in Turkey. In an epidemiolo-
gical survey, Werber et al. (2005) isolated S. Oranienburg from 18 (5%)
of 381 the tested chocolates during the outbreak period that occurred in
Germany in 2001. Nascimento et al. (2015) also found that 150 cocoa
products samples (30 samples of each of nibs, liquor, cocoa cake, cocoa
butter and cocoa powder), with pH values of 5.3–7.4, and aw of
0.29–0.52, collected from two different cocoa processing industries in
Brazil were negative for E. coli and Salmonella. However, other En-
terobacteriaceae were detected. In a national survey in Canada, Salmo-
nella spp. And generic E. coli were not detected in 3173 samples of
chocolate-based confectionaries collected from retail markets in 11 ci-
ties between 2016 and 2018, while coliforms were found in 44 samples
(1.4%) at levels ≥ 1.8 MPN/g (Canadian Food Inspection Agency,
CFIA, 2019). Other foodborne pathogens including E. coli, S. aureus and
L. monocytogenes have also been reported to contaminate OL aw food
products (Alaouie et al., 2017; Yamani and Isa, 2006).
4. Illness outbreaks and recalls linked to OL aw foods
In recent years, low aw foods or food ingredients have been asso-
ciated with foodborne illness outbreaks due to contamination with
foodborne pathogens. Unfortunately, several pathogens can persist in
low aw foods for months, or years, in concert with static health hazard
(Beuchat et al., 2013).
The persistence of pathogens in the foods increases with decreasing
aw and increasing fat content (Santillana Farakos et al., 2013). Food-
borne pathogens that survive in low aw foods showed higher resistance
to other treatments including heat compared to pathogenic cells grew in
high aw environments (Gurtler et al., 2014).
The origin of pathogens in low aw food depends on how it is
6
Food Microbiology 92 (2020) 103571
prepared, in other words, whether the food is comprised of several
components or added to an already processed food. In contrast, direct
ingestion is possible following consumption of raw material without
processing or if raw material is added to a processed product. Other
foods might be processed by heating or cooking before being consumed.
Some pathogens may originate pre- or post-harvest, during processing
or post-processing (Podolak et al., 2010). In this section, some selected
outbreaks of illnesses and global recalls associated with LO aw foods are
presented. Foodborne illness outbreaks or product recalls associated
with LO aw foods have been reported for S. enterica, enterohaemor-
rhagic E. coli, L. monocytogenes, Bacillus cereus, Clostridium (Cl.) botu-
linum, Cl. perfringens, Cronobacter sakazakii and other pathogens
(Beuchat et al., 2013).
Salmonella can persist under dry conditions in food processing
plants and foods (Gurtler et al., 2014). Foodborne outbreaks of sal-
monellosis associated with peanut butter, tahini and halva are reported
in Table 1. Salmonella can survive in tahini and tahini halva during its
shelf life and could cause illness upon consumption (Lake et al., 2010;
Osaili et al., 2017, 2020). A number of foodborne illnesses between
2002 and 2003 were traced back to imported tahini contaminated with
S. Montevideo in Australia and New Zealand (Unicomb et al., 2005).
Salmonella from different parts of the globe were recorded in tahini
from Saudi Arabia in 1982–1983 (Ayaz et al., 1986) and in halva from
England and Wales in 2001 (Willis et al., 2009) and Turkey in 2005
(Kahraman et al., 2010). Also, recalls of tahini or halva were recorded
in Canada (CFIA, 2013; 2015, 2016), France, Spain, Switzerland, the
Netherlands, the US and the UK (Harris et al., 2019). Furthermore,
more than 15 Salmonella serotypes were identified in high fat foods in
New Zealand between 2000 and 2009 (Lake et al., 2010). Recalls due to
the possibility of Salmonella contamination in processed peanuts were
reported in many countries during the period 2006–2010 including
Belgium, Cyprus, Denmark, Greece, Hungary, Iceland, Italy, Jamaica,
Lebanon, the Netherlands, Portugal, Romania, Spain, Sweden, Trinidad,
Turkey, Norway and other countries. A recall due to Salmonella was
reported in Canada during 2013 and 2015 involving chocolate-based
confectionaries (CFIA, 2019). In the US, 5,141 food products with low
aw were recalled during 2007–2012 because of contamination with
bacterial pathogens (FDA, 2012a). During this period, worldwide, 41
low aw food outbreaks caused 7,315 illnesses with 536 hospitalizations
and 63 deaths (Santillana Farakos et al., 2013). Salmonella was the most
common isolate, being responsible for 94% of food recalls in the US and
53% of these worldwide outbreaks (Santillana Farakos et al., 2013).
Among these recalls in the US, three main recalls were reported in 2009
involving dry milk, peanut butter products and pistachio nuts. In 2012,
Salmonella-contaminated peanut butter resulted in 41 cases in 20 states
(FDA, 2012a). In 2013, outbreaks with S. Montevideo and S. Mbandaka
in tahini were also reported in the US (CDC, 2013b).
Contamination of tahini with L. monocytogenes is also a safety
concern as this bacterium is widely distributed in the environment and
can survive in foods stored under refrigeration. To-date, although there
have not been any reported outbreaks, there have been a number of
recalls due to L. monocytogenes contaminated low aw foods (Ly et al.,
2019). In New Zealand, a recall of tahini due to contamination with L.
monocytogenes without reported illnesses has been recorded
(eFoodAlert, 2008). Boiled peanuts were associated with Cl. botulinum
type A in Taiwan in 1986 (Chou et al., 1988) and in Canada in 2012 as
recorded by Sheppard et al. (2012). In the US, a Shiga toxin producing
E. coli strain was also linked to soy nut butter product when 5 (31%)
patients developed hemolytic uremic syndrome (FDA, 2017).
5. Survival of pathogenic bacteria in OL aw foods
The growth or survival of pathogenic bacteria in food products is
affected by various factors including the chemical and physical prop-
erties of foods (intrinsic features), storage conditions or extrinsic fea-
tures, implicit features which include the physiological properties of
A.N. Olaimat, et al.
microorganisms, as well as processing features such as heating, can-
ning, and irradiation (Jay, 2000; Yousef and Courtney, 2003). The
major intrinsic factors affecting behavior of pathogens in OL aw foods
are the low aw and the presence of a high content of fat. Although OL aw
food products do not support growth of foodborne pathogens, several
studies reported the ability of major bacterial pathogens to survive in
tahini (Al-Nabulsi et al., 2014, 2013; Olaimat et al., 2017b; Osaili et al.,
2020; Torlak et al., 2013), halva (Kotzekidou, 1998; Sengun et al.,
2005; Osaili et al., 2017), peanut butter (Burnett et al., 2000; He et al.,
2011; Kataoka et al., 2014; Kenney and Beuchat, 2004; Kilonzo-
Nthenge et al., 2009; Park et al., 2008) and chocolate (Podolak et al.,
2010; Tamminga et al., 1977) for long storage periods.
5.1. Survival of foodborne pathogens in tahini
Salmonella is the most important pathogenic bacteria occurring in
OL aw foods because it has been responsible for several illness out-
breaks. Studies have shown that Salmonella spp. have a characteristic
ability to survive in these products for long periods. Torlak et al. (2013)
found that a cocktail of three serotypes of Salmonella (S. Typhimurium,
S. Newport and S. Montevideo) survived up to 16 weeks in tahini with
an aw of 0.17 at 22 or 4 °C with reductions of 4.5 and 3.3 log CFU/g,
respectively. Al-Nabulsi et al. (2014) also found that S. Typhimurium
survived in tahini with an aw of 0.31 up to 28 d, where numbers were
decreased by 3.3, 2.3 and 1.7 log CFU/g at 37, 21 and 10 °C, respec-
tively, at 28 d. E. coli O157:H7 and L. innocua behaved similarly in
tahini(aw = 0.31); they were able to survive well up to 28 d at different
temperatures, although the latter was more resistant. Numbers of E. coli
O157:H7 and L. innocua were reduced by 4.9 and 3.2 log CFU/ml at
37 °C, 3.0 and 2.0 log CFU/ml at 21 °C; and 2.5 and 1.1 log CFU/ml at
10 °C, respectively, after 28 d (Al-Nabulsi et al., 2013). In another
study, numbers of S. aureus also decreased in tahini with an aw of 0.33
by 3.3, 1.6 and 0.7 log CFU/g at 37, 21 and 10 °C, respectively (Olaimat
et al., 2017b). Recently, Osaili et al. (2020) found that that numbers of
unstressed or desiccated-, heat-stressed Salmonella decreased as the
storage temperature and time increased or the aw of tahini decreased.
The unstressed Salmonella serotypes (S. Cubana, S. Aberdeen, S. Ty-
phimurium, and S. Paratyphi) cocktail survived well in tahini samples
adjusted to aw of 0.17, 0.35 or 0.50 for at least 12 and 9 months at 10
and 25 °C, respectively, regardless of aw level. Exposure of Salmonella
cells to desiccation stress before inoculation in tahini reduced their
survivability; while heat stress had no significant effect.
It is evident that the survival of pathogens is significantly influenced
by the storage temperature and bacterial type, where the lower bac-
terial reductions occurred with Gram-positive bacteria (S. aureus and L.
innocua), particularly at low temperatures which may suggest that re-
duced metabolic activity at lower temperatures enhances their ability to
survive well in OL aw foods for lengthy periods. Gram positive bacteria
lack an outer membrane, but they are surrounded by a peptidoglycan
layer which is thicker than that in Gram negative bacteria and this may
enhance their ability to survive longer in these products. In addition,
teichoic acids and surface proteins play a crucial role in survival of
Gram positive bacteria in hostile environments (Silhavy et al., 2010).
On the other hand, when tahini was hydrated to 10% in distilled
water to yield an aw of 0.93–0.95, S. Typhimurium, E. coli O157:H7, S.
aureus and L. innocua grew well and numbers of S. Typhimurium, S.
aureus and E. coli O157:H7 increased by 4.1, 3.9 and 3.3 log CFU/g at
37 °C, 3.2, 3.0 and 5.7 log CFU/g at 21 °C and 3.0, 1.8 and 5.9 log CFU/
g at 10 °C, respectively, at 28 d (Al-Nabulsi et al., 2013, 2014; Olaimat
et al., 2017b). L. innocua was not recovered on PALCAM agar at 37 °C
after 3 d, although it was recovered on TSA overlaid with PALCAM
agar, which suggested that rehydrated tahini caused metabolic stress
and injury to L. innocua cells. Moreover, 3.1 log CFU/ml injured L. in-
nocua cells were recovered after 28 d at 21 °C, while no injured cells
were observed at 10 °C. However, only ≤0.6 log CFU/ml E. coli
O157:H7 injured cells were observed in hydrated tahini at all storage
7
Food Microbiology 92 (2020) 103571
temperatures (Al-Nabulsi et al., 2013). It is likely that the tahini-based
products such as hummus, and eggplant dip (mutabal) with high aw and
suitable content of nutrients do not cause bacterial injury and can fa-
cilitate the growth of foodborne pathogens (Al-Holy et al., 2006;
Olaimat et al., 2017a; Osaili et al., 2015).
5.2. Survival of foodborne pathogens in halva
Few studies have investigated the behavior of pathogenic micro-
organisms in halva. Sengun et al. (2005) reported that a high inoculum
(5.3 log CFU/g) of S. aureus survived in halva having an aw of 0.17 with
bacterial reductions at 9 months of 2.7 and 3.2 log CFU/g at 4 and
20 °C, respectively. When the initial inoculum was reduced to 3.1 log
CFU/g, S. aureus cells were not detected after 1 or 2 months of storage
at 4 and 20 °C, respectively. In another study, Kotzekidou (1998) found
that S. Enteritidis survived in air-sealed or vacuum-packed halva con-
taining 31.8% fat and an aw of 0.18 for up to 8 months at 6 and 20 °C,
with a reduction of ≤1.4 log CFU/g, while superior survival was ob-
served in the vacuum-packaged halva. More studies examining the
survival of foodborne pathogens in halva are required. Recently, Osaili
et al. (2017) investigated the effect of heat and desiccation on the
survival of Salmonella spp. in halva during 12 months storage at 10 and
25 °C. They found that unstressed, desiccation- or heated-stressed Sal-
monella spp. were reduced by 2.7, 2.6 or 2.8 log CFU/g, respectively,
after 12 months at 10 °C; however, at 25 °C the Salmonella reductions
were higher, reaching 5.2, 6.7 or 6.3 log CFU/g, respectively, at the end
of storage. It was notable that heat and desiccation significantly de-
creased the survival of Salmonella during the last 3 months of storage at
25 °C.
5.3. Survival of foodborne pathogens in peanut butter
Peanut butter-based products are mainly made of peanuts, oil, and
other ingredients such as salt, sugar, and stabilizers. Fat content may
vary from 6 to 54% (vol/vol) depending on the product type (He et al.,
2011). Because of different ingredient formulations, there are wide
differences in the survival pattern of foodborne pathogens. Burnett
et al. (2000) studied the survival of high (5.7 log CFU/g) or low (1.5 log
CFU/g) inocula of a 5 serotype Salmonella (S. Typhimurium, S. Mon-
tevideo, S. Michigan, S. Enteritidis and S. Agona) cocktail in 5 com-
mercial peanut butters (aw = 0.20 to 0.33) and two peanut butter
spreads (aw = 0.22 to 0.28). They found that the numbers of Salmonella
with high inoculum in peanut butter and peanut butter spreads de-
creased by 4.1–4.5 log CFU/g at 21 °C and 2.9 to 4.3 log CFU/g at 5 °C
after 24 weeks of storage. In the low inoculum peanut butter and
spreads Salmonella was detected by enrichment in all samples except
natural peanut butter with no stabilizers after storage for 24 weeks at
5 °C; however, at 21 °C, with the exception of one peanut butter spread
product, all tested samples were negative for Salmonella. The order of
products regarding their ability to allow greater Salmonella survival was
peanut butter spreads > traditional (regular) peanut butter >
reduced sugar, low-sodium peanut butter > natural peanut butter.
In another study, Park et al. (2008) reported that numbers of S.
Tennessee in 5 commercial brands of peanut butter (47–50% fat,
19–22% carbohydrate and 0.28–0.47% salt with an aw of 0.17–0.25)
decreased by only < 1.3 log CFU/g after 2 weeks of storage at 4 °C or
22 °C. He et al. (2011) studied the survival of a cocktail containing 5
Salmonella serovars and 5 E. coli O157:H7 strains in peanut butter
products with different formulations. They found that numbers of Sal-
monella and E. coli O157:H7 decreased by ≤ 1.0 log CFU/g in regular
peanut butter with an aw of 0.4 (33.3% fat and 41.7% carbohydrate)
after 4 weeks of storage at 4 or 25 °C. In an organic peanut butter (with
or without salt) having a similar aw but different fat and carbohydrate
contents (50% fat and 21.9% carbohydrate), the reduction in bacterial
recovery increased from 2.5 to 3.0 log CFU/g for Salmonella and 3.2 to
5.0 log for E. coli O157:H7 after 4 weeks of storage at 25 °C. But at 4 °C,
A.N. Olaimat, et al.
the bacterial reduction was < 1.7 for S. enterica and 2.7 for E. coli
O157:H7. The presence of 0.25% salt in peanut butter increased the
susceptibility of E. coli O157:H7 at 25 °C, while no additional effect was
observed against Salmonella. In a reduced fat peanut butter
(fat = 6.25%) with higher aw (0.7) and salt (0.59%), numbers of Sal-
monella and E. coli O157:H7 were reduced by 3.5 and 1.4 log CFU/g,
respectively, after 4 weeks at 25 °C, while at 4 °C, ≤ 0.7 log CFU/g was
observed for both pathogens (He et al., 2011). It seems that the com-
bination of high aw and high storage temperature enhances the bac-
terial reduction in peanut butter even with low fat concentrations
(6.25%). Kilonzo-Nthenge et al. (2009) reported that numbers of Sal-
monella and E. coli O157:H7 in a commercial peanut butter decreased
by 1.1 log CFU/g and 2.8 log CFU/g, respectively; after 15 weeks of
storage at 4 °C. While at 25 °C, numbers of both pathogens were lower
than the detection limit (1.0 log CFU/g), but they were found using the
Reveal® complete system kit. It is obvious that the bacterial reductions
increased as the storage temperature increased.
Kenney and Beuchat (2004) found that numbers of L. monocytogenes
were reduced by 2.4–3.8 log CFU/g in chocolate-peanut spread and
peanut butter (with aw values adjusted to 0.33 and 0.65, respectively)
stored at 20 °C for 24 weeks. Survival of L. monocytogenes was enhanced
in products with the lower aw even though the pathogen was not
completely eliminated during this period. Clavero et al. (2000) also
found that numbers of Cl. botulinum decreased by ≤ 0.9 log CFU/g in
peanut spread with aw values of 0.92–0.98 stored at 30 °C under
anaerobic conditions for 16 weeks. It was noticed that visible fermen-
tation signs occurred on peanut spread with an aw of 0.96 and 0.98
within 3 d of storage, which may have increased the CO2 concentration
and enhanced growth of C. botulinum.
It is believed that exposure of microorganisms to stress during food
processing enhances their ability to tolerate other stresses which may
improve their survival in food products under different conditions (Al-
Nabulsi et al., 2015; McMahon et al., 2007; Osaili et al., 2008). Kataoka
et al. (2014) investigated the survival of heat-stressed S. Typhimurium,
S. Tennessee, and Enterococcus faecium in 4 formulations of peanut
paste combined with two aw levels (0.3 and 0.6) and two fat levels (47
and 56%). They found that numbers of S. Tennessee, S. Typhimurium,
and E. faecium were reduced after 12 months storage at 20 °C by
1.3–2.4, 1.8–2.8, and 1.1–2.1 log CFU/g, respectively, in these pro-
ducts. They also confirmed that pathogen survival was enhanced in
pastes with lower aw, although the fat level showed no significant effect
on the survival of pathogens.
To explain the better survival of pathogenic microorganisms in
peanut butter having lower aw, it has been suggested that bacterial cells
aggregate around the water droplets in these products and thus make a
protective colloidal suspension of lipids and water. The size of water
droplets affects the survival of foodborne pathogens where larger dro-
plets produced by the coalescence of water in peanut butter at lower aw
enhances pathogen survival for longer periods than in oily products
with higher aw which may support stability of the emulsion. Ingredients
in these products including fat, sugar, salt and other solutes may also
partially contribute to the survival of foodborne pathogens for long
periods. In general, pathogen survival decreased with high storage
temperatures, lower carbohydrate content, higher sodium, and higher
fat content (Burnett et al., 2000; He et al., 2011; Kataoka et al., 2014;
Kenney and Beuchat, 2004).
5.4. Survival of foodborne pathogens in chocolate
Similar to other OL aw products, Salmonella is the bacterial pathogen
of greatest public health concern in chocolate and chocolate-containing
products because they have too often been linked to illness outbreaks
due to their consumption over the last 4 decades (ICMSF, 2011;Werber
et al., 2005; Bean and Post, 2014; Gutiérrez, 2017). Further, it is evi-
dent that cocoa is among the food products associated with significant
human salmonellosis outbreaks (Nascimento et al., 2015). Low
8
Food Microbiology 92 (2020) 103571
concentrations of Salmonella (0.005–23 CFU/g) have been found in
chocolate products involved in foodborne illness outbreaks which un-
derlines the importance of these pathogens to survive for long periods
in chocolate products (Hockin et al., 1989; Werber et al., 2005). It has
been documented that Salmonella can persist in chocolates for > 9
months at room temperature (Podolak et al., 2010). Tamminga et al.
(1977) reported that S. Typhimurium and S. Eastbourne were able to
survive and were detectable in chocolate for up to 15 and 19 months,
respectively, at room temperature. In another study, different serovars
of Salmonella survived well on raw ingredients (cocoa butter oil, cru-
shed cocoa and hazelnut shells, cocoa beans) used in the manufacture of
chocolate products stored at 5 or 21 °C for 21 d (Komitopoulou and
Penaloza, 2009). Tsai et al. (2019) reported that L. monocytogenes was
able to survive in natural unsweetened cocoa powder with an aw of 0.30
for 12 months at 22 °C. However, as the aw increased the survival of the
pathogen decreased. Kenney and Beuchat (2004) found that whole fat
(4.0%) and reduced fat (1.0%) chocolate milks supported growth of L.
monocytogenes at 10 and 22 °C. Further, the pathogen was able to sur-
vive in a chocolate-peanut spread (39% fat with an aw of 0.33 or 0.65)
up to 24 weeks at 20 °C.
6. Bacterial responses and mechanism of survival in OL aw foods
Although there are some suggested methods by which bacteria
present in an OL aw food can survive such harsh conditions, the exact
mechanisms of survival are not well understood (Finn et al., 2013a).
Upon exposure to the osmotic stress of low aw foods, bacteria try to
overcome the stress by increasing intracellular concentrations of com-
patible solutes, which balance the osmolarity of the intracellular en-
vironment with that externally and thus prevent water loss. Osmopro-
tectants are accumulated inside bacterial cells without adversely
affecting enzymatic activity. Low molecular weight compatible solutes
such as ectoine, proline and glycine-betaine are concentrated in-
tracellularly to resist water loss (Csonka, 1989). Trehalose is a dis-
accharide osmoprotectant, which was suggested to be crucially im-
portant for the osmoadaptation of E. coli, C. sakazakii and Salmonella
(Barron and Forsythe, 2007; Finn et al., 2013a; Strøm and Kaasen,
1993). It is thought that the transport and production of osmoprotec-
tants is dependent on the initial increase of intracellular K+ con-
centration. Balaji et al. (2005) reported that the kdp genes encoding for
K+ transport were found to be produced many fold higher when cells
were exposed to osmotic stress. Upregulation of kdp genes in response
to osmotic stress leads to increased release of potassium glutamate,
which stimulates buildup of osmoprotectants (Lee and Gralla, 2004). It
was postulated that the ability of Cronobacter species to persist under
low aw conditions could be attributed to its ability to form biofilms and
produce extracellular polysaccharides along with cell-to-cell signaling
molecules, which may contribute to the ability of the organism to adapt
to living in a stressful environment (Beuchat et al., 2013). However, it is
not known whether the same factors would contribute to bacterial
persistence in fatty, low aw foods.
In a high fat food environment, it is believed that fatty acids provide
for efficient ATP production per carbon atom and hence cells can spare
glucose, which will be then diverted toward trehalose biosynthesis. It
was indicated that genes responsible for fatty acid catabolism were
upregulated when Salmonella cells were exposed to desiccation stress
(Finn et al., 2013a; Li et al., 2012). Additionally, an upregulation of
three transporter genes (ProP, ProU and OsmoU) occurred, which were
shown to provide a major contribution to Salmonella resistance under
low aw stress conditions in a liquid system (Finn et al., 2013b). Fur-
thermore, Sigma factors (σS and σE) have also been linked to increased
tolerance of Salmonella to dehydration and osmotic stress (Finn et al.,
2013a). Additionally, a mechanism called DNA supercoiling was also
suggested to contribute to the overproduction of ProU, and an ABC-
transporter involved in accumulating osmoprotectants necessary to
tolerate osmotic stress (Finn et al., 2013b). In one study in which S.
A.N. Olaimat, et al.
Enteritidis was inoculated in peanut butter with an aw of 0.3, the or-
ganism entered a partially dormant state as exemplified by limited
(< 5%) genome transcription compared to 78% when the same bac-
terium was cultured in Luria-Bertani broth (Deng et al., 2012). A
completely dormant state was also was reported for Salmonella in re-
sponse to stress, where Salmonella had adapted to osmotic stress by
entering a viable but non-culturable (VBNC) state (Oliver, 2010), in
which the cells are not recoverable by regular laboratory procedures.
Yet, these cells still have the potential to recover and reach infectious
doses, when favorable growth conditions re-occur (Gupte et al., 2003).
Additionally, it was reported that certain genes which are usually
turned on in response to heat and cold shock or provide DNA protec-
tion, also contributed to increased survival of Salmonella under low aw
in peanut oil (Deng et al., 2012).
It is worth noting that exposure of pathogens such as Salmonella and
E. coli O157:H7 to a low aw, high fat environment can provide such
pathogens the opportunity to cross-protect themselves against other
common stresses used to control pathogens in food production en-
vironments. Kataoka et al. (2014) reported that prior exposure of bac-
terial cells to stressors such as heat or desiccation appears to provide
cross-protection for bacterial cells to low aw, high fat exposure. Gruzdev
et al. (2011) found that desiccation-stressed S. enterica showed in-
creased resistance to UV irradiation, dry heat, sanitizing agents and bile
salts, but was more susceptible to organic acid. Increased heat tolerance
as exhibited by larger indices of thermal inactivation kinetics (D and Z
values) were shown by Salmonella and E. coli O157:H7 present in LO aw
foods such as peanut butter (He et al., 2011; Podolak et al., 2010). In
foods such as halva and tahini, which are characterized by hyper-
osmolarity, E. coli O157:H7 was found to respond to such stressful
conditions by accumulation of compatible solutes regulated by σS or by
altering its enzymatic activity. Other regulons including σ32 and σE are
also activated by hyper osmolarity and code for chaperones and pro-
teases that enable proper protein assembly under stress conditions
(Bianchi and Baneyx, 1999; Osaili et al., 2018a).
Fat content plays a role in providing protection for some pathogens
present in milk with unnaturally high fat (10%). It was reported that
cream diluted to 10% fat protected L. monocytogenes and E. coli
O157:H7 better than milk with ≤7% fat when treated using ohmic
heating (viability of treated S. Typhimurium was the exception and was
unaffected by fat level). Notably, the electrical conductivity was lower
in the cream with 10% fat. It is possible that at relatively high fat levels,
large fat globules will form hydrophobic zones which will not be heated
in the same manner as its surroundings. Hence, pathogens present in-
side the fat-enriched zones will be less subject to heating and may
possibly exhibit a better chance of survival (Kim and Kang, 2015). Also,
in other work C. sakazakii inoculated into whole milk exhibited more
resistance to x-ray treatment as shown by a higher D-value compared to
reduced fat and skim milks (Mahmoud, 2009). Nonetheless, increasing
the fat content of milk to 10–15% with cream was reported to increase
the sensitivity of inoculated L. monocytogenes to the lethal effect of high
hydrostatic pressure. Increasing the fat content of milk might have led
to increasing the concentration of lipid soluble substances that possess
antilisterial activity and may have altered the permeability of microbial
cell membranes (Roig-Sagués et al., 2009).
The entry of bacterial cells into the VBNC state has also been sug-
gested as one of the mechanisms for survival of pathogens in LO aw
foods. Additionally, Salmonella cells are thought to form clumps inside
or on the surface of water droplets in peanut butter allowing them to
withstand its low aw (0.3) and high fat (47–56%) for as long as 12
months (Kataoka et al., 2014). Syamaladevi et al. (2016) reported in-
creased thermal resistance of microorganisms present in OL aw foods
and higher values of thermal inactivation parameters were also re-
ported for bacterial cells previously exposed to desiccation stress.
Salmonella showed greater survival in chocolate when added as a
dry inoculum than when added as a liquid (Tamminga et al., 1976). It
was also postulated that the high fat content of chocolate may protect
9
Food Microbiology 92 (2020) 103571
pathogenic bacterial cells against gastric juices and thereby increase the
chance for entrance and colonization of the GIT (Finn et al., 2013a).
7. Control of bacterial pathogens in OL aw foods
Contamination of OL aw products with foodborne pathogens may
occur during pre-processing, processing or post-processing steps
(Olaimat and Holley, 2012). Therefore, control of pathogens in these
products is necessary at each step of potential contamination: in the
field, during harvesting, processing, distribution, retail markets, food-
service facilities, or at home to improve the safety of these products
(Beuchat et al., 2013; Frank, 2014). However, preservation treatments
still need to be applied to eliminate pathogens that may be present in
these products (Syamaladevi et al., 2016). In this review, the applica-
tion of practices and methods to reduce pathogen contamination during
or after processing is examined. These practices include controlling the
quality of raw materials and ingredients and applying good agri-
cultural, manufacturing, and hygienic practices at each step in the
processing chain (Frank, 2014). Moreover, interventions such as che-
micals, natural antimicrobials, thermal inactivation, high pressure,
gamma and electron beam (e-beam) irradiation are evaluated to in-
activate foodborne pathogens in OL aw products.
7.1. Thermal inactivation
An essential step in the production of tahini, halva, peanut butter
and chocolate is the roasting of sesame seeds, peanuts or cocoa beans,
to enhance the desired flavor, color and texture and thus improve the
overall palatability of these products. A variety of time-temperature
combinations are used in roasting processes (Kahyaoglu and Kaya,
2006; Torlak et al., 2013; Gutiérrez, 2017). Torlak et al. (2013) found
that roasting of sesame seeds at combinations of 110 °C for 60 min,
130 °C for 50 min, or 150 °C for 30 min, completely inactivated a 3
serovar cocktail of Salmonella (S. Typhimurium, S. Newport and S.
Montevideo) inoculated at 5.9 log CFU/g. Similarly, Doyle (2009) re-
ported that the roasting of peanuts at combinations of 129 °C for
45 min, 146 °C for 15 min, and 163 °C for 10 min reduced Salmonella
numbers by 4.3, 4.9 and 5.3 log CFU/g, respectively. It has also been
reported that roasting of cocoa beans at high temperatures
(110–130 °C) can eliminate Salmonella and other enteric bacteria
(ICMSF, 2011; Nascimento et al., 2012). It seems that typical roasting of
seeds (≥130 °C for 60 min) is sufficient to eliminate foodborne pa-
thogens such as Salmonella spp.; however, the contamination of OL aw
products may take place after this heat treatment, and underlines the
need to expose the final product to pasteurization before packaging.
Heat treatment of peanut butter at 70–90 °C reduced the viability of
several Salmonella serovars (Agona, Typhimurium and Enteritidis) in
peanut butter by only 1.4–2.5 log CFU/g and 2.7–3.0 after 5 and
20 min, respectively; while after that bacterial numbers did not de-
crease significantly at any temperature, even after 50 min. When
peanut butter was inoculated with the cocktail at 4.5 log CFU/g, similar
bacterial reductions of 1.5–2.6 log CFU/g were obtained at all three
temperatures after 5 min (Shachar et al., 2006). Mattick et al. (2001)
reported that Salmonella numbers were reduced by only 1.5 log CFU/g
in peanut butter heated at 55 °C for 98 min, 65 °C for 48 min, or 74 °C
for 6 min. Kenney and Beuchat (2004) investigated the thermal toler-
ance of L. monocytogenes in peanut butter containing 53% fat with an aw
of 0.31, and they found that the D-value at 60 °C was 26 min. Keller
et al. (2012) reported that the D-values of S. Tennessee and S. Or-
anienburg in peanut butter heated at 85 °C were 12.0 and 12.8 min,
respectively. Nascimento et al. (2012) reported that Salmonella was
more resistant to heat at 110–130 °C in chocolate nibs than in cocoa
beans. The D-values were 8.9, 8.0, 3.8 min in nibs and 4.8, 3.6, 2.6 min
in cocoa beans at 110, 120 and 130 °C, respectively. He et al. (2011)
studied the effect of heat treatment on the viability of desiccation-
stressed cells of S. enterica and E. coli O157:H7 inoculated in peanut
A.N. Olaimat, et al.
butter for 30 d before heat treatments. They found that the numbers of
both S. enterica and E. coli O157:H7 were reduced by only < 2 log CFU/
g when heated at 72 °C for 60 min in peanut butter with an aw of 0.4
and 33% or 50% fat content. In contrast, heat treatment at 90 °C for
60 min reduced both bacterial numbers by 5.5–7.1 log CFU/g in peanut
butter containing 33% fat and by 3.2–5.2 log CFU/g in peanut butter
containing 50% fat. Additionally, they observed that thermal in-
activation of desiccation-stressed S. enterica in peanut butter took
longer than non-stressed cells which confirmed that stressed cells were
more resistant to heat treatment. Kataoka et al. (2014) reported that
exposing contaminated peanut paste having different aw (0.3 and 0.6)
and fat content (47% and 56%) to heat treatment at 75 °C for 30 min
reduced numbers of S. Tennessee, S. Typhimurium and E. faecium by
1.5–2.7, 1.5–3.0 and 0.4–1.4 log CFU/g, respectively. They observed
that the tested bacteria showed more resistance as aw decreased. Si-
milarly, He et al. (2013) found that increased aw and decreased fat
content in peanut butter significantly reduced the heat resistance of
desiccation-stressed S. Enteritidis, S. Typhimurium and S. Tennessee
treated at 90 or 126 °C. It has been reported that Salmonella cells can be
protected in specific microenvironments in the peanut butter suspen-
sion due to high fat. Moreover, phenotypic changes in surviving cells
that have been exposed to environmental stresses such as desiccation
may enhance the thermal resistance of microorganisms (He et al., 2013;
Shachar et al., 2006). Nonetheless, low aw, water mobility, high lipid
content, physiological state of microorganisms and other factors may
affect the pasteurization efficacy and increase bacterial resistance
which may suggest the need for use of other methods.
It is worth mentioning that while the conching step can cause
substantial reductions in the numbers of pathogens during processing of
chocolate, this step is insufficient to control Salmonella in chocolate or
its products (Krapf and Gantenbein-Demarchi, 2010; Nascimento et al.,
2012). Krapf and Gantenbein-Demarchi (2010) found that D-values for
Salmonella spp. were 245 and 306 min at 50 and 60 °C, respectively, in
cocoa butter. D-values were 999 and 26 min at 50 and 90 °C, respec-
tively, in cocoa liquor, and D-values were 1574 and 25 min at 50 and
90 °C, respectively, in dark chocolate. They found z-values of 14 and
20 °C in cocoa liquor and dark chocolate, respectively. In another study,
Nascimento et al. (2012) reported that conching of milk chocolate
caused a rapid death rate in Salmonella during the first 3 h followed by a
lower inactivation rate until 24 h. D-values for the first 3h were 217,
102, and 51 min and for the period of 3–24 h were 1077, 482 and
702 min at 50, 60 and 70 °C, respectively.
7.2. Natural antimicrobials
Few studies have investigated the incorporation of natural anti-
microbial agents to control foodborne pathogens, particularly
Salmonella, in OL aw foods (Al-Nabulsi et al., 2014; Chen et al., 2015;
Olaimat et al., 2017b). The addition of ≤0.5% acetic acid or citric acid
to commercial tahini with an aw of 0.3 reduced S. Typhimurium by
2.7–4.8 log CFU/ml and 2.5 to 3.8 log CFU/ml, respectively, at 37, 21
and 10 °C after 28 d. Viable bacterial cells were not detected in hy-
drated tahini with an aw of 0.95 containing 0.5% acetic acid or citric
acid after 7 and 21 d, at the tested temperatures (Al-Nabulsi et al.,
2014). In another study, the addition of 0.5% citric or acetic acid de-
creased numbers of S. aureus by ≤ 2.3 log CFU/ml in commercial tahini
at 37, 21 and 10 °C after 28 d compared to the control. While in hy-
drated tahini, S. aureus cells were not detectable with addition of 0.3 or
0.5% acetic acid after 28 and 14 d, respectively, at 10 °C; and after 14
and 7d, respectively, at both 21 and 37 °C. It was also found that viable
bacteria were not detected after 14 and 28 d at 21 and 37 °C, respec-
tively, when tahini was treated with 0.1% acetic acid. Bacterial cells
were also reduced to the undetectable limit by 21 d at the tested tem-
peratures when tahini was treated with 0.5% citric acid, or by 28 and
21d, with 0.1 and 0.3% citric acid, respectively, at 21 °C (Olaimat et al.,
2017b). Al-Nabulsi et al., 2020 found that incorporation of 2.0%
10
Food Microbiology 92 (2020) 103571
cinnamon or thyme oil into commercial tahini reduced numbers of E.
coli O157:H7 by 1.4–2.2 log10 CFU/ml after 28 d at all storage tem-
peratures (37, 25 or 10 °C). In hydrated tahini, E. coli O157:H7 cells
were not detected after 21 d at all storage temperatures when 1%
cinnamon oil was added or after 28 d at 37 and 25 °C when 1% thyme
oil was added.
Chen et al. (2015) evaluated the antimicrobial activities of carva-
crol, cinnamaldehyde, and lauricarginate (LAE) against S. Tennessee in
peanut paste containing low (< 5%) or high (50%) fat content and with
different aw. They found that 2500–5000 ppm carvacrol reduced
numbers of S. Tennessee by 4.3–5.5 and 3.6–4.7 log CFU/g in low fat
peanut paste with an aw of 0.3 and 0.5, respectively, after 3 d at 25 °C.
Salmonella cells were not detected in either product (> 6 log CFU/g
reductions) with 1250–2500 ppm cinnamaldehyde (after 5 d) or
5000 ppm LAE (after 1 d) at 25 °C. However, 2500 ppm cinnamalde-
hyde, 5000 ppm LAE or their combination reduced S. Tennessee num-
bers by 3.4, 4.1 and 5.8 log CFU/g in peanut paste containing 50% fat
with an aw of 0.33–0.35 after 5 d at 25 °C. It seems that natural anti-
microbials have the potential to reduce the risk of foodborne pathogens
in OL aw foods; however, further studies are required to evaluate the
organoleptic characteristics and overall acceptability of these in-
gredients by consumers.
7.3. Gamma and electron beam irradiation
Gamma irradiation is an alternative to heat treatment for inactiva-
tion of bacterial pathogens in foods which is considered safe and ef-
fective by the U. S. Food and Drug Administration (FDA) for use in
meat, poultry, spices, fresh fruits, and vegetables (Ban and Kang, 2014;
FDA, 2009a). The effectiveness of gamma irradiation for the inhibition
of foodborne pathogens in OL aw products including peanut butter,
tahini and halva has been evaluated (Ban and Kang, 2014; Osaili et al.,
2016, 2018b; Osaili and Al-Nabulsi, 2016). Ban and Kang (2014) found
that exposure of peanut butter having different aw (0.18, 0.39, and
0.65) to gamma irradiation reduced numbers of a 3 strain cocktail of S.
Typhimurium by 1.3–1.9, 2.6 to 2.8, and 3.5 to 4.0 log CFU/g at doses
of 1, 2, and 3 kGy, respectively. Osaili et al. (2016) reported that
numbers of unstressed, starvation-stressed, and heat-stressed Salmonella
cells in a cocktail (S. Typhimurium, S. Aberdeen, S. Cubana, and S.
Paratyphi) present in tahini containing 58.1% fat with an aw of 0.19,
were reduced by 4.5–4.7 log CFU/g using gamma irradiation at a dose
of 2.0 kGy, while numbers of cold-stressed Salmonella were reduced 4.5
log CFU/g after exposure to 0.6 kGy. In another study of similar com-
mercial tahini, an irradiation dose of 1 kGy reduced a 5 strain E. coli
O157:H7 cocktail (unstressed, heat-, cold-, starvation-, salt-, acid-, al-
kaline- or ethanol-stressed cells) by 2.6–3.2 log CFU/g (Osaili and Al-
Nabulsi, 2016). Osaili et al. (2018a) found that the D-values of tahini
samples stored for 0–30 d at room temperature before irradiation
treatment were 1.5–1.8, 1.3 to 1.5 and 0.9–1.3 kGy for Salmonella spp.,
E. coli O157:H7, and L. monocytogenes, respectively. The storage of ir-
radiated samples further reduced all bacterial numbers
by ≥ 2 log CFU/g during 30 d, and in addition, E. coli O157:H7 cells
were eliminated from the samples until of the end of storage. In another
study, Osaili et al. (2018b) investigated the effect of desiccation and
heat stresses on the resistance of Salmonella spp., L. monocytogenes and
E. coli O157:H7 to gamma irradiation in halva. They found that de-
siccation stress significantly reduced the gamma radiation resistance of
Salmonella and L. monocytogenes, while heat stress significantly in-
creased the resistance of E. coli O157:H7 and L. monocytogenes and
significantly reduced the resistance of Salmonella. In cocoa husks, ir-
radiation at 5 kGy was effective in reducing numbers of En-
terobacteriaceae, coliforms, and Streptococcus D to undetectable levels
(Bonvehí and Isal, 2000). Similarly, Granados et al. (2016) found that
irradiation at 3–5 kGy inhibited growth of Salmonella spp., Enterobacter
hormaechei and Klebsiella pneumonia in cocoa beans.
Hvizdzak et al. (2010) reported that electron beam radiation at a
A.N. Olaimat, et al.
dose of 0.5–3 kGy reduced numbers of S. Tennessee and S. Typhi-
murium in creamy peanut butter with an aw of 0.51 and fat content of
53% by 4.1–6.75 log CFU/g and 2.9 to 4.9 log CFU/g, respectively. It is
likely that gamma and electron beam irradiation could be used as ef-
ficient methods for control of bacterial pathogens in OL aw foods (Ban
and Kang, 2014; Osaili and Al-Nabulsi, 2016; Osaili et al., 2018b).
7.4. Hydrostatic pressure
Another alternative to thermal processing in the food industry that
has gained more attention in recent years is high pressure processing
(HPP). Grasso et al. (2010) evaluated the efficacy of HPP, using a dose
of 600 MPa at 45 °C for 5 min to decrease S. Typhimurium inoculated
into peanut butter. They found that there were no significant reductions
(P > 0.05) in S. Typhimurium numbers in treated peanut butter
compared to untreated samples. Similarly, D'Souza et al. (2014) showed
that exposing peanut butter with different aw levels to HPP at 600 MPa
for 18 min caused limited reduction in the viability of a cocktail of 6
Salmonella strains. They found that at an aw ~0.16 (50% added peanut
oil), a statistically (but not practical) significant, 0.8 log reduction was
achieved while no significant log reduction was observed when the aw
was reduced to ~ 0.13 through the use of 75% peanut oil. Moreover,
they reported that ~1 log reduction was obtained in peanut flour, while
a 2 log CFU/g reduction was observed in peanut oil. When HPP was
combined with nisin, a 1.7 log CFU/g reduction was achieved. In an-
other study, D'Souza et al. (2012) studied the effect of pressure cycling
under three sets of conditions involving 3 to 10 cycles of pressure from
400 to 600 MPa, and hold times of 6 min on the inactivation of a
cocktail of S. Enteritidis PT30, S. Tennessee, S. Oranienburg, S. Anatum,
S. Enteritidis PT 9c and S. Montevideo in a creamy peanut butter. They
observed only ≤2 log reduction compared to the initial concentration
of 6.5 log CFU/g, regardless of the HPP pressure-time conditions used.
Salazar et al. (2019) reported no significant reduction in the population
of L. monocytogenes in tahini treated with 350 MPa for 4 min or with an
additional treatment of 600 MPa for 10 min. It is obvious that the use of
HPP for inactivation of foodborne pathogens in OL aw had only very
limited success compared to reductions in survival of foodborne pa-
thogens reported in high moisture food. Combining HPP with mild heat
treatment (50–60 °C) may enhance its activity and reduce the protective
effect of high fat content in OL aw products.
8. Sanitation, hygienic design of manufacturing facilities, good
hygienic practices, environmental monitoring
OL aw producers are required to find means to prevent the occur-
rence of pathogenic organisms in their finished products. The potential
hazards and risks throughout the manufacturing stages of these pro-
ducts could be eliminated through implementation of planned ap-
proaches of food safety management systems such as the International
Organization for Standardization (ISO) 22000, good manufacturing
practices (GMP), Good Hygienic Practices (GHP), and Hazard Analysis
Critical Control Points (HACCP) systems to evaluate, manage, and
control the potential hazards and produce OL aw products free from
different types of hazards (Beuchat et al., 2013; International Com-
mission on Microbiological Specifications for Foods, ICMSF, 2011).
Potential hazards points can be identified at exact steps. Once
identified, these hazards can be prevented, or reduced to safe levels.
The hazardous points in a food process include ingredients, premises,
equipment, plant environments, practices or procedures (Kandhai et al.,
2004; Shaker et al., 2007). Protective control procedures to prevent
contamination of chocolate during manufacturing are crucial. Im-
plementation of cleaning and sanitation of equipment and premises,
hygienic design of manufacturing facilities, good hygienic practices,
and environmental monitoring in the OL aw establishment play a cri-
tical role in preventing product contamination with pathogens, with a
greater focus on post-processing steps or products that are not subjected
11
Food Microbiology 92 (2020) 103571
to processing steps such as heat treatment (Food and Agriculture
Organization & World Health Organization, FAO/WHO, 2015).
Poor sanitation and maintenance of equipment may become po-
tential sources of microbial contamination during processing steps
(Burndred and Peace, 2017). These conditions have been linked to
salmonellosis outbreaks in peanut butter in the U.S. (FDA, 2012b).
Therefore, peanut butter processing industries should be prepared to
include adequate sanitary facilities and accommodations such as water
supply, toilet facilities and hand wash stations. Further, all sections of
the plant such as walls and ceilings, fixtures, equipment, and utensils
and other physical components like heating and ventilation equipment
(HVAC) should be effectively and regularly cleaned and sanitized to
prevent initial and cross-contamination with foodborne pathogens
(FDA, 2009b; GMA, 2009; Podolak et al., 2010; Scott et al., 2009). For
example, equipment and utensils used in chocolate manufacturing
should be designed to permit effective cleaning by different solutions
and temperatures. Liquid handling equipment should be made to drain
freely. Handling of dry ingredients may generate dusty materials, and
therefore should be moved in closed systems equipped with dust control
features that collect and eliminate dusty particles from the processing
areas (Canadian Food Inspection Agency, CFIA, 2014).
In processing low moisture foods, the traditional wet-cleaning
methods are not recommended for use because they may introduce
moisture to the products which promotes the growth of foodborne pa-
thogens. Therefore, dry sanitation methods are safest and should be
used in the processing of low moisture foods (Beuchat et al., 2013).
Grasso et al. (2015) suggested use of hot oil (90 °C) for 2 h followed by
60% isopropanol for 1 h which was an effective treatment to eliminate
Salmonella from contaminated peanut butter processing equipment.
Ingredients should be held and kept under controlled conditions to
minimize microbial activity and prevent cross-contamination. The
National Academy of Science (1969) indicated that ingredient testing is
considered the first important step in food manufacturing to minimize
or prevent pathogenic organisms like Salmonella from being proble-
matic in finished food products. In OL aw manufacturing, obtaining raw
materials from reliable suppliers is necessary. Monitoring of raw ma-
terials transport and storage upon receipt at the manufacturing facility
and minimizing the potential of cross-contamination between the raw
materials and the finished product are also important measures to
preclude the presence of the pathogens in the end product (Podolak and
Podolak and Black, 2017).
It is essential to halt entry of foodborne pathogens via insects and
rodents into the low moisture processing establishment by im-
plementation of proper hygienic design standards for such premises,
including room, layouts, zoning, equipment, process space and infra-
structure (Beuchat et al., 2013; FAO/WHO, 2015; Gilmour, 2009; GMA,
2009). Physical barriers, such as doors, walls, and split conveyors
should be used to separate the processing environment from other areas
including receiving, handling and pre-processing of raw material areas,
waste areas, maintenance areas, and toilet facilities. The appropriate
design of ventilation systems and airflow in establishments should
control entry of dust. Moreover, these establishments also should be
designed to enable dry cleaning and the use of appropriate disinfection
methods in processing areas (FAO/WHO, 2015; GMA, 2009; Scott et al.,
2009).
Good hygienic practices among food establishment employees can
influence the safety of foods. When Enterobacteriaceae, especially coli-
forms, have been isolated from process areas, food handlers have fre-
quently been the most likely source for contamination of these areas
and finished products (Nascimento et al., 2015). Large numbers of ill-
ness outbreaks have resulted from poor hygienic practices (Beuchat
et al., 2013). Therefore, strict personal hygienic measures should be
enforced and be consistent with GMPs which can be achieved through
training. Monitoring employee practices in the principles of food pro-
tection and handling techniques such as the potential sources of food
contamination and the importance of sanitation and hygiene practices
A.N. Olaimat, et al.
including general cleanliness, hand washing, and hair covering must
also be an integral part of acceptable programs (FAO/WHO, 2015; Scott
et al., 2009).
Finally, an environmental monitoring program to ensure that pro-
ducts and food contact surfaces with high risk of contamination are
frequently sampled and tested for presence of pathogens should be es-
tablished in low moisture food industries. Trend analysis of samples
such as food contact surfaces, air, dust plus finished food samples are
important to verify the effectiveness of control measures such as good
hygienic practices and cleaning and sanitation (FAO/WHO, 2015; GMA,
2009).
9. Conclusions
OL aw products have been routinely associated with large illness
outbreaks and recalls, particularly involving Salmonella spp. The re-
markable ability of some foodborne pathogens to survive in OL aw food
products for long periods is commonly observed and is due to the high
levels of fat in these foods. Although these low aw products are usually
exposed to heat treatment during processing, which is sufficient to
eliminate pathogens from the seed or seed coat, post-processing con-
tamination may take place during other stages of processing. It is evi-
dent that foodborne pathogens can often find their way into OL aw
foods and may survive longer in low aw and dry foods than in foods
with higher aw. Intervention strategies should focus on prevention of
bacterial contamination, which is usually a much greater challenge
than finding effective control measures. Therefore, the most effective
approach to prevent pathogen contamination should be based on sa-
nitation-related procedures; implementation of efficient cleaning and
hygienic measures in the food plant environment.
10. Further studies
The general strategy for contamination prevention is to understand
the mechanism well enough by which contamination and disease
transmission can occur to interrupt them. Therefore, the effective ap-
plication of control requires coordinated effort among those responsible
for harvesting, processing and distribution activities. It is evident that
study is required to more fully characterize the main routes by which
pathogen contamination occurs in these products during production in
the field and during processing.
The ultimate goal should be to increase our knowledge of pathogen
behavior in OL aw foods by developing and implementing control
measures that will decrease the frequency of illnesses associated with
this food category. In this review, the ability of some decontamination
processes, including some natural antimicrobials and irradiation for
control of foodborne pathogens in these foods has been summarized.
However, other natural antimicrobials such as essential oils of different
plants should be evaluated in depth for their action against pathogens
in OL aw foods. The combination of natural antimicrobials with physical
methods such as irradiation, HHP and UV light could also be in-
vestigated. Further, there is a lack of surveillance data on foodborne
pathogens in OL aw foods. National and international surveys are re-
quired to assess the potential for consumption of contaminated OL aw
products to cause illnesses. Efforts are needed to increase the sensitivity
of assay techniques to recover desiccated cells of pathogenic micro-
organisms and isolate them from food when present in very low num-
bers. Few studies have assessed stressed bacterial cells for their survival
and strategies for their control in OL aw foods by comprehensively in-
vestigating the behavior of stressed foodborne pathogens in these pro-
ducts in response to challenge by gamma or e-beam irradiation and
selected natural antimicrobials while controlling fat, carbohydrate and
moisture content of the foods tested.
12
Food Microbiology 92 (2020) 103571
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
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