Sources and Risk Factors for Contamination, Survival, Persistence, and Heat Resistance of Salmonella in Low-Moisture Foods

Review

Sources and Risk Factors for Contamination Survival Persistenceand Heat Resistance of Salmonella in Low-Moisture Foods

RICHARD PODOLAK ELENA ENACHE WARREN STONE DARRYL G BLACK AND PHILIP H ELLIOTT

Grocery Manufacturers Association 1350 I Street NW Suite 300 Washington DC 20005 USA

MS 09-513 Received 24 November 2009Accepted 2 June 2010

ABSTRACT

Sources and risk factors for contamination survival persistence and heat resistance of Salmonella in low-moisture foods are

reviewed Processed products such as peanut butter infant formula chocolate cereal products and dried milk are

characteristically low-water-activity foods and do not support growth of vegetative pathogens such as Salmonella Significant

food safety risk might occur when contamination takes place after a lethal processing step Salmonella cross-contamination in

low-moisture foods has been traced to factors such as poor sanitation practices poor equipment design and poor ingredient

control It is well recognized that Salmonella can survive for long periods in low-moisture food products Although some die-off

occurs in low-moisture foods during storage the degree of reduction depends on factors such as storage temperature and product

formulation The heat resistance of Salmonella is affected by many factors mostly by strain and serotypes tested previous growth

and storage conditions the physical and chemical food composition test media and the media used to recover heat-damaged

cells Salmonella heat resistance generally increases with reducing moisture Care must be taken when applying published D- and

z-values to a specific food process The product composition and heating medium and conditions should not be significantly

different from the product and process parameters used by the processors

Low water activity (aw) is a barrier to growth for many

vegetative pathogens including Salmonella spp (11)Processed products such as powdered milk chocolate

peanut butter infant foods cereal and bakery products are

characteristically low-water-activity foods (35 80 92 109126) While these products do not support the growth of

Salmonella all have been implicated in outbreaks of

salmonellosis (22ndash24 31 71 105 110) Epidemiological

and environmental investigations of these outbreaks have

suggested that cross-contamination plays a major role in the

contamination by Salmonella of these products (22ndash24 31105 110)

Cross-contamination is the transfer of bacteria from one

surface object or place to another (91) Significant food

safety risk might occur when transfer of a pathogen takes

place where the product is ready to eat with no additional

Salmonella inactivation step in the process (103) In a 2004

review article Reij et al (103) cited a survey conducted by

the World Health Organization (132) which indicated a

significant proportion of European foodborne outbreaks

could be traced back to cross-contamination The report

indicated that factors contributing to the presence of

pathogens in prepared foods included insufficient hygiene

(16) cross-contamination (36) processing or storage

in inadequate locations (42) contaminated equipment

(57) and contamination by personnel (92) In a

compilation of outbreaks in the United Kingdom where

the contributing factor was known cross-contamination

accounted for 57 of all occurrences (99) In order to

minimize the risk of salmonellosis from the consumption of

low-moisture foods it is crucial for manufacturers to apply

best efforts to control various risk factors that could lead to

cross-contamination

It is expected that Salmonella may be present in or on

any raw food materials (10) in part because Salmonella is

widespread in nature Salmonella can survive for weeks in

water and for years in soil if environmental conditions such

as temperature humidity and pH are favorable (120)Because of its ubiquitous nature Salmonella may cycle

through a host into the environment and back into another

host eg through animals to soil and water and back to

animals through contaminated water and food (32 45 131)Studies showed that Salmonella may survive in dry

foods and feeds for a long time (60 65 67) Janning et al

(65) studied the survival of 18 bacterial strains (including

Salmonella) under dry conditions (aw of 02) at 22uC After

an initial decrease in cell numbers the Salmonella strains

evaluated remained stable for a very long time and 248 to

1351 days were needed to achieve a 1-log reduction

Salmonella was more resistant to desiccation under the

experimental conditions than were Enterobacter cloacaeand Escherichia coli Hiramatsu et al (60) investigated the

ability of Salmonella spp to survive under dried conditions

on paper disks with an aw of 05 to 06 and in selected dry

foods such as dried squid chips and plain dried squid They Author for correspondence Tel 202-637-8052 Fax 202-639-5993

E-mail rpodolakgmaonlineorg

1919

Journal of Food Protection Vol 73 No 10 2010 Pages 1919ndash1936Copyright G International Association for Food Protection

reported that the survival of dried Salmonella cells

substantially increased (up to 79 times) when sucrose

(36) was present in a desiccation model system compared

with one without sucrose Survival of Salmonella spp

inoculated in dried squid chips containing sucrose was 23 to

89 times greater than that in the dried paper disks whereas

the populations of Salmonella in dried plain squid without

sucrose were almost equal to those in the dried paper disks

(60) The authors also reported that Salmonella in the

presence of sucrose might survive for months in foods such

as chocolate peanut butter and potato chips The

combination of high fat and low water activity might have

a synergistic effect on Salmonella survival (60)The heat resistance of Salmonella in low-moisture

products is affected by many factors (37) These include

factors prior to heating (eg growth medium composition

growth phase growth temperature and stress such as heat or

acid) and factors during heating (eg acidity fat content

and addition of solutes to the matrix as well as the

Salmonella strains used) (56) Heat resistance observed in

an aqueous system is not applicable to a low-moisture

product For example a study by Ng and colleagues (94)found that Salmonella Senftenberg 775W was the most heat

resistant among 300 strains evaluated in an aqueous solution

(Salmonella Senftenberg 775W was 30-fold more resistant

than was any other strain evaluated) while this strain was

found to be less heat resistant than Salmonella Typhimur-

ium in chocolate (49) Salmonella Enteritidis PT30 the

target organism for raw almonds was implicated in an

outbreak and was found to be more resistant to dry heat than

were many of the strains evaluated on almonds (3 127)The aim of this review is to provide insights into the

sources and risk factors for contamination by Salmonella in

low-moisture products and to address the survival and heat

resistance of the pathogen with specific references that may

be used to help to develop the appropriate formulations and

processes for these products

SOURCES AND RISK FACTORS FORCONTAMINATION BY SALMONELLA IN

LOW-MOISTURE PRODUCTS

Salmonella contamination in low-moisture foods has

been traced to poor sanitation practices substandard facility

and equipment design improper maintenance poor opera-

tional practices and good manufacturing practices (GMPs)

inadequate ingredient control and other factors Many such

instances are not documented in the literature This section

summarizes and analyzes those reports that have been

published

Contamination associated with poor sanitationpractices Poor cleaning and sanitation is often cited as a

contributing factor in many outbreaks of foodborne illness

The risk of cross-contamination has been considered lower

when food contact surfaces are dry partly because bacterial

growth and survival would be reduced However Salmo-nella may be able to survive dry conditions on surfaces for

extensive time Kusumaningrum et al (75) demonstrated

that in the case of Salmonella the effects of cross-

contamination due to poor sanitation practices are enhanced

by the organismrsquos ability to survive on dry surfaces for

extended time and then transfer to foods on contact The

authors showed that Salmonella Enteritidis remains viable

on dry stainless steel surfaces and presents a potential for

contamination for considerable time Salmonella Enteritidis

was readily transferred from these test surfaces to foods

with transfer rates of 20 to 100 Salmonella Enteritidis

was recovered from dry highly contaminated (105 CFU

cm2) stainless steel surfaces for at least 4 days and for 24 h

from moderately contaminated surfaces (103 CFUcm2)

This is significant because after undertaking cleanup and

sanitation activities manufacturers typically initiate new

production much sooner than the times in these timetables

studied by Kusumaningrum et al (75) Residual concentra-

tions of organisms used in the above study should not be

found in a well-run establishment but if they are cross-

contamination potential would be high due to the transfer

rate cited here

During investigations into outbreaks of salmonellosis

evidence of Salmonella has been found in plant processing

environments (3 15 40 123ndash125) where sanitation

appeared substandard An outbreak of Salmonella Agona

associated with toasted oat cereal prompted examination of

potential cross-contamination in the processing areas air-

handling systems ingredients and traffic flow of the

manufacturing factory Investigators found widespread low

levels of the organism in the plant environment including

samples taken from the floor production equipment and the

exhaust system in the plant (15) The investigators

concluded that the unsanitary condition of the equipment

(especially the air-handling systems) poor employee

practices and poor control of the vitamin spray mixing

and holding process (eg multiple dead legs direct

connection of the vitamin supply line to the potable water

supply without maintaining proper backflow protection)

were ongoing factors with the potential to produce

contamination in the cereal product (123) An investigation

of Salmonella Senftenberg contamination in infant cereal

revealed that bulk cereal was contaminated with lsquolsquocleaning

remainsrsquorsquo from milling machinery (105) Investigations into

two consecutive Salmonella Enteritidis outbreaks in bakery

products (43) showed that the second outbreak was most

likely due to poor equipment sanitation Piping nozzles used

daily for making fresh cream cakes were inadequately

cleaned potentially allowing cross-contamination

Morita et al (93) studied the mechanisms of Salmonellacontamination in a Japanese oil meal (rapeseed or canola

meal) factory The authors found Salmonella on many

environmental vectors including operators processing area

floors dust in the air and rodents In particular high

concentrations of Salmonella were found in samples with

high oil content from the floor of the manufacturing area

The authors concluded that high Salmonella contamination

rates for the processing area represented the greatest risk for

cross-contamination of the oil meal They also stated that

restricting the movement of operators remarkably reduced

Salmonella contamination In a study involving contami-

nated chocolate by Craven et al (31) investigators

1920 PODOLAK ET AL J Food Prot Vol 73 No 10

recommended reducing opportunities for Salmonella East-

bourne cross-contamination by controlling airborne spread

of dust Butcher and Miles (20) also indicated that dust was

a major source of Salmonella contamination of poultry feed

in processing mills

In Moritarsquos study (93) which sought to identify

potential vectors of contamination in a Japanese oil meal

factory the authors also developed quantitative data and

determined from this data that restricting the movement of

manufacturing operators could have a very positive effect in

reducing the spread of Salmonella They documented that

100 of manufacturing workers shoes and 90 of their

work gloves were contaminated with Salmonella after being

effectively disinfected within 1 day The authors also

determined that 65 of floor swabs were Salmonellapositive These findings clearly supported the authorrsquos

conclusion that restricting the movement of operators

between factory areas (eg receiving versus manufacturing

versus storage) and disinfecting the bottoms of work shoes

when moving between zones is needed to prevent the spread

of the organism

Contamination associated with poor facility andequipment design and inadequate maintenance Cross-

contamination because of sanitary practice failures is not

always attributed to procedural and human errors In some

cases the manufacturing equipment is of poor sanitary

design andor has not been properly installed or maintained

Poor facility and equipment design and machinery mainte-

nance can also contribute to the problem of Salmonellacontamination

Improper facility and equipment design as well as

maintenance issues at a companyrsquos processing plant were

observed by government investigators in response to a 2008

to 2009 nationwide outbreak of Salmonella Typhimurium

associated with various peanut products in the United States

(123) In one case investigators observed open gaps as

large as 05 in (127 cm) by 25 ft (762 cm) at the air

conditioner intakes located in the roof of the facility There

were several indications that rainwater had been leaking into

the factory The gaps were located in the productionndash

packaging room and totes of finished roasted product and a

packaging line were located directly underneath the gaps

In the same inspection investigators noted other

equipment and facility design issues that could have

contributed to cross-contamination at the plant (123) A

felt material was present on a final machine roller at the

peanut roasterrsquos discharge Felt is a material that cannot be

adequately cleaned and sanitized In addition it was noted

that the facility was not equipped with a ventilation system

that would provide airflow from the factoryrsquos finished goods

section to the raw receipt and staging area from its more

sanitary sections towards the less hygienic areas Such a

design often termed lsquolsquopositive pressurersquorsquo creates higher air

pressure in parts of a factory after a lethality step has been

applied versus those areas where raw nonprocessed goods

are stored or staged A positive pressure system prevents

contaminated air originating in raw product areas from

escaping to other parts of the facility

Improper equipment and facility design was also a

probable culprit in other salmonellosis outbreaks In a report

on investigations following an international outbreak of

Salmonella Eastbourne where 200 people were affected by

contaminated chocolates produced at a Canadian factory

Craven et al (31) indicated that raw cocoa beans were the

probable source of Salmonella which survived the heating

step during production It was also suggested that valves in

conches were arranged such that chocolate that had not been

heated could accidentally be pumped directly to a finished

product storage tank In addition investigators cited

inadequate separation between clean and unclean zones as

a causative factor for potential product adulteration During

Breuerrsquos (15) investigation into a Salmonella Agona

outbreak associated with toasted oat cereal the investigators

found poor facility design in the implicated factory where a

majority of the equipment was open to the atmosphere The

authors characterized cleaning and sanitation as lsquolsquovery

difficultrsquorsquo because insufficient space was allocated between

pieces of equipment Morita et al (93) research in the

Japanese oil meal factory demonstrated that choice of

flooring material could be critical in factory design The

researchers tested different disinfection methods on diverse

types of flooring material They found that regardless of the

disinfectant used with three different application methods

rough concrete could not be effectively rid of SalmonellaIn response to outbreaks of the past 10 years the

Grocery Manufacturers Association (53) recently published

a sanitary equipment design checklist for low-moisture

foods The utilization of these principles may help minimize

equipment design flaws improve sanitation effectiveness

and minimize the risk of product contamination and

outbreaks (15 31 123)In the Craven report (31) designing processing hardware

such that unprocessed material can bypass the lethality

(cooking) step is a devastating oversight It is hoped that this

case can serve as a caveat to future engineers and designers

Any suspicion that a process bypass could occur must be

investigated comprehensively and thoroughly The outbreak

reported by Craven et al (31) occurred 35 years ago The

industry now has much more sophisticated control mecha-

nisms available which may be employed to prevent process

bypasses This can be a prudent design expense that can

deliver repeated payback by preventing product bypass over

the related public health consequences

Even the most impeccably designed equipment and

facilities can become sources of Salmonella contamination

if they are not properly maintained The source of

Salmonella Ealing in an outbreak associated with infant

dried milk was traced to poor equipment maintenance A

factory spray dryer had a hole in its inner lining which

allowed the escape and return of powder from the dryerrsquos

contaminated insulation material (104) In another outbreak

in England 37 cases of foodborne illness during the spring

and summer of 2006 caused by Salmonella Montevideo

were linked to internationally distributed chocolate prod-

ucts The manufacturer attributed the contamination to a

leaking pipe at one of its main factories (14) In a 2007

outbreak of Salmonella Tennessee infections associated

J Food Prot Vol 73 No 10 SALMONELLA AND LOW-MOISTURE FOODS 1921

with peanut butter in the United States a company

spokesperson indicated that the outbreak was traced to

problems with a leaky roof and two instances of faulty

sprinklers being activated (46) US Food and Drug

Administration (FDA) investigations of the outbreak

included collecting samples from the plant environment

(134) One hundred twenty-two environmental samples

were collected by the FDA and two tested positive (a floor

squeegee sample and a drain sample from the roaster room)

According to Zink (134) lsquolsquowater event(s)rsquorsquo in the facility

might have increased the numbers of Salmonella and led to

product contamination

In addition to the potential microbial contaminants

introduced from poor equipment and facility design and

maintenance issues such as leaky roofs leaking pipes and

faulty sprinklers these events introduced moisture into a

normally dry environment Moisture control is critically

important in preventing Salmonella contamination in low-

moisture products (63) Water in the dry processing

environment is one of the most significant risk factors for

Salmonella contamination because the presence of water

allows the pathogen to grow in the environment where

normally the lack of moisture would prevent this The

subsequent growth caused by the introduction of moisture

significantly increases the risk for product contamination

Moisture most likely contributed to the cross-contamination

in the United Kingdom chocolate (14) and US peanut

butter (46) outbreaks by facilitating the growth of otherwise

dormant Salmonella that might have come from the

aforementioned sources

Contamination associated with lack of GMPsProcessors especially those supplying products that will

receive little or no further lethality treatment from

consumers need to be aware of potential contamination

hazards and employ GMPs to fully protect the health of their

customers Food manufacturers must thoroughly evaluate

their operations and provide appropriate mitigations based

on those hazards presented by their unique situations

Without these mitigation protocols cross-contamination

could occur and resulted in adulterated goods even when a

lethality step is used in the process The following case

demonstrates such a situation

In 2001 halvah a candy made from sesame seeds and

sugar was implicated in an international outbreak of

Salmonella Typhimurium DT 104 (16) As a follow up to

this outbreak Brockman et al (16) examined several

sesame products for the occurrence of the pathogen In

addition to finding Salmonella Typhimurium in the halvah

involved in the outbreak researchers also found different

Salmonella Typhimurium strains in halvah from other

manufacturers and other countries As part of this same

study the authors also uncovered Salmonella Offa

Salmonella Tennessee and Salmonella Poona in tahini

(sesame paste) and sesame seeds While sesame seeds can

be contaminated with Salmonella during growth of the

seeds storage or processing the researchers stated that the

organism should not survive during the production of

halvah because of the high temperatures (120 to 140uC) that

are used in the preparation milling and hot mixing

processes of the candy manufacture Consequently they

concluded that the likely cause of the outbreaks was cross-

contamination of the halvah after the heat treatment step

(55) This certainly is a plausible scenario and a prudent

manufacturer should have operational and GMP controls in

place to prevent such an occurrence Even though the

temperatures involved in halvah processing appear similar

to other reported literature values for obtaining multilog

reductions of Salmonella (4 84 109) the authors did not

specify if the halvah process was validated to achieve a

particular log reduction of Salmonella Quantifying such

information would have lent more credence to the

conclusion that the presence of the organism in the halvah

was due to cross-contamination

Contamination associated with poor ingredientcontrol and handling Even a well-designed equipment

systems operating with detailed preventive maintenance

programs and comprehensive operational practices cannot

combat cross-contamination from poor choice sourcing

and control of raw materials and ingredients Contaminated

ingredients used in products without a further kill step could

carry the pathogen directly into finished products For

example paprika powder contaminated with multiple

serovars of Salmonella used in the manufacture of

paprika-powdered potato chips was implicated in an

estimated 1000 cases of salmonellosis (78) Poor choice

of formulation ingredients can have similar detrimental

results Marshmallows made with raw egg whites resulted in

36 cases of Salmonella Enteritidis PT4 infections (80)In still further examples Koch et al (72) investigated a

Salmonella Agona outbreak in Germany and reported that

the organism was found among products from 12 producers

of herbal teas that contained aniseed The contaminated

aniseed was traced to a single importer who indicated that

the source of the contamination was a single batch of

aniseed (cultivated in Turkey) that had been fertilized with

manure Hedberg et al (57) reports a case where

Salmonella-contaminated cheese was supplied to four

separate shredding operations While better sanitation

practices at the shredding plants might have minimized

the scope of the problem these plants essentially were

dealing with contaminated ingredients supplied by another

company which resulted in finished products contaminated

with Salmonella Javiana In June of 2007 the FDA warned

consumers not to consume a low-moisture childrenrsquos snack

food due to possible contamination with SalmonellaWandsworth (124) By mid-July the Centers for Disease

Control and Prevention had identified 60 people mostly

toddlers from 19 states who had become ill Five were

hospitalized but no deaths were reported An FDA

consumer update (124) indicated that the seasoning mix

used in the snack food might have been the source of the

contamination In the aforementioned Rushdy et al (105)investigation of eight reported cases of Salmonella Senften-

berg infections in infants which occurred in 1995 in

England the illness was associated with the consumption of

one brand of baby cereal One of the companyrsquos suppliers


used common machinery to process heat-treated bulk cereal

ingredients and other products that were not heat treated

The receiving company in spite of receiving a previous

shipment of bulk cereal contaminated with SalmonellaSenftenberg did not thoroughly investigate the supplier and

did not identify the ingredient as a possible source of

Salmonella in their finished product During the supplierrsquos

risk assessment the supplier failed to identify the use of

common machinery as a potential source for introduction of

Salmonella into the processing equipment system and

therefore did not have control measures in place to mitigate

this risk

Ingredient control is not limited to programs designed

to ensure the procurement and delivery of clean and

wholesome raw materials Once these materials are

received they must be stored and handled in a manner that

does not enhance opportunities for cross-contamination

Poor handling in fact has lead to cross-contamination even

in products subject to a lethality step Poor control of

ingredients that potentially contain Salmonella can allow it

to colonize a facility resulting in the organism finding its

way into fully processed finished products In the US

nationwide outbreak of Salmonella contamination associat-

ed with peanut products (125) mentioned above FDA

investigators noted raw peanut storage and staging areas that

were housed in the same open room with no segregation as

finished product handling equipment Finished goods

packaging operations were also located near raw peanut

handling with no segregation The FDA observed that totes

of raw peanuts were stored directly next to totes of finished

roasted peanuts In another situation environmental inves-

tigations conducted in response to an outbreak found

contamination risks existed within tree nut processing

facilities and on farms (41 63) An outbreak of SalmonellaEnteritidis associated with raw almonds occurred in Canada

and the United States in 2000 and 2001 (41 64) Salmonellawas found in 16 of 32 orchard samples All of the growers

involved indicated that manure or biosolids were not used

on the land within the previous 5 years No livestock or

poultry farms were nearby However Salmonella of the

same phage type found in the orchards was isolated from

environmental samples collected from the processing

equipment where 25 of equipment swabs cultured

positive It was postulated that Salmonella from field

contamination colonized the plant environment and the

processing equipment which in turn could have contami-

nated almonds during processing

In the Rushdy study (105) the authors cite the baby

cereal supplierrsquos hazard analysis and critical control point

(HACCP) system for failure to identify a potential hazard in

their hazard analysis However in 1995 HACCP was in its

developmental stages (114) Today many HACCP practi-

tioners include an in-depth and thorough evaluation of

potential contamination sources from their suppliers in

addition to those that might occur internally Tools

employed in this analysis could include on-site inspections

review of HACCP plans requirements for certificates of

analysis indicating the supplierrsquos goods have tested negative

for Salmonella and ingredients (93) Implementation of

such an approach today may help minimize the potential

hazards identified by Rushdy et al (105) 15 years ago and

prevent such hazards from entering the supply chain thus

minimizing the risk of product contamination and outbreaks

Pest control and Salmonella contamination Pest

control is an important food safety program in all

manufacturing facilities While the literature reviewed does

not contain any documented cases where pest activity was

directly implicated in Salmonella cross-contamination there

are studies that show that common rodents and insects can

be vectors for Salmonella transmission

In the previously cited study by Morita et al (93) the

researchers captured autopsied and analyzed the stomach

contents of 48 rodents caught over the period of 1 year in a

Japanese factory Of rodents captured from the manufac-

turing area 46 tested positive for Salmonella while

rodents captured from the receiving and storage areas all

tested negative Seven different serovars were found in

those rodents testing positive along with several untypeable

strains

In a study involving seven species of common grain

insects Crumrine et al (32) demonstrated that SalmonellaMontevideo was transmitted by insects from inoculated

wheat to clean wheat The authors concluded that insects

contaminated with Salmonella Montevideo could contam-

inate large masses of grain In yet another study Kopanic et

al (73) found that cockroaches are capable of acquiring and

transmitting Salmonella Typhimurium and therefore are

potential vectors of the pathogen Furthermore infected

cockroaches were capable of infecting other cockroaches

The identification of three different pest-oriented

potential vectors (rodents cockroaches and grain insects)

clearly indicates that pest control is not a program that can

be ignored in a well-designed Salmonella-prevention

strategy The mobility of these insects and rodents could

easily aid in widely transferring Salmonella throughout a

facility from what was formerly an isolated niche

Sources and risk factors summary This review

demonstrates that cross-contamination by Salmonella can

occur in a variety of low-moisture foods from an assortment

of sources and vectors In many of these cases the causative

factor was determined to be a single cause and in some

situations multiple factors were responsible Manufacturers

would be well served to identify potential sources of

contamination and implement control measures against

these

The publication by Rushdy et al (105) demonstrates the

potential for the breakdown of several pathogens mitigation

strategies when potential problems are not addressed by the

manufacturer First the company had a breakdown in their

HACCP system by not recognizing the potential problems

that could be introduced by their suppliers Then in spite of

receiving a batch of bulk cereal that contained SalmonellaSenftenberg from their vendor the company still did not

take steps to address the supplierrsquos food safety and pathogen

mitigation strategies and continued to use ingredients from

this supplier Had they investigated the situation with more


intensity they would have discovered an incomplete

supplier HACCP program poor equipment and facility

design (common equipment for cooked and noncooked

goods) and poor sanitation practices (bulk cereal contam-

inated with cleaning remains) Finally the company

approached their food safety programs in this manner while

manufacturing a product baby cereal which targets an

immunosensitive population

SURVIVAL OF SALMONELLA INLOW-MOISTURE FOODS

Salmonella can easily adapt to extreme environmental

conditions such as lower or higher than optimal tempera-

tures pH values or desiccation Although the optimal

growth temperature is 35 to 37uC Salmonella can grow at

temperatures as low as 2uC and as high as 54uC (12) While

the optimal pH for growth of Salmonella is in the range of

65 to 75 growth has been observed at pH levels between

38 and 95 (12 83 128) In general it is considered that no

growth of pathogenic bacteria occur below approximately

an aw value of 085 (83) but an aw as low as 093 is

sufficient to support growth of Salmonella (12) When these

conditions are below outside growth conditions Salmonellamay survive for months or even years in certain low-

moisture foods It was reported that survival and heat

resistance of microorganisms increases as aw decreases (1862 69 87) Although water activity plays a major role

Goepfert et al (50) stated that survival of the organism

during heating is a function of a medium composition rather

than water activity of the surrounding environment In the

same dry conditions survival of Salmonella spp may vary

depending on food matrix and medium composition (35 4959 60 92) Air-dried Salmonella cells in which water

activity is lowered without the use of solutes become more

heat tolerant Cells dried to an aw 057 for 48 h showed

increased resistance but no significant change in shape of

the survival curves occurred with longer periods of

dehydration Although a loss of viability was observed it

was attributed to the lethal damages occurring during the

process of dehydration (70) It was demonstrated that while

an aw of 065 protected Salmonella at temperatures as high

as 70uC or greater it promoted more rapid cell destruction at

lower temperatures (86) Hills et al (59) hypothesized that

the microbial stability of a food may be improved by

manipulating the food microstructure of air-water distribu-

tion making the water and nutrients unavailable to

microbial cells To prevent growth of Salmonella it is

important to keep the available water below the growth

threshold so that cells that survive the initial osmotic shock

phase will be unable to multiply and eventually die off due

to starvation

Several authors reported that reduced water activity has

a protective effect against the inactivation of Salmonella in

different food products such as cake mix peanut butter

chocolate chocolate syrup skim milk onion soup

flummery flour dried squid chips dry milk and cocoa

powder (6 29 60 67 87 109 129) While the water

activity is an important controlling factor of microbial

growth and survival other factors such as medium

composition (ie solutes used to decrease the water

activity) (50 60) or the microscopic air-water distribution

in foods (59) might be as or more important as the water

activity itself

Chocolate and confectionary products Finished

chocolate is probably the most consumed confectionary

product in the world and has a very low moisture content

(8) and an aw of 04 to 05 (10) In the last few decades

chocolate products have been implicated in a number of

salmonellosis outbreaks (10 31 48 51 61 68 107 129)In some cases very low levels of contamination (1 to 3 cells

per g) were detected in the finished product (31 34 51)Kapperud et al (68) did not exclude the possibility that

contaminated particles containing many viable Salmonellacells could be unevenly distributed in the product and that

the infections were caused by large doses of Salmonellainstead of small doses The latter scenario was considered

less likely because of the thorough mixing of the chocolate

at the factory It has been suggested that the high fat content

of chocolate may protect Salmonella cells against the action

of gastric acid in the stomach which allows the cells to

colonize the lower gastrointestinal tract and produce clinical

symptoms even when a very small number of the cells is

present in the product (31 34 50)Although Salmonella cannot grow in finished choco-

late it can survive for a long time and it represents

significant risk even at low levels of contamination (34)Barrile and Cone (8) found that lyophilized cells of

Salmonella Anatum inoculated into milk chocolate at levels

of 50 cells per 100 g was detected at a level of 14 most

probable number (MPN)100 g after 15 months of storage at

room temperature Tamminga et al (117) demonstrated that

Salmonella might survive for months in different types of

chocolate (Table 1) The chocolate industry faces a difficult

task in controlling Salmonella for a variety of reasons

which include (i) raw materials and ingredients such as raw

cocoa beans or powdered milk may carry Salmonella (ii)

low water activity and high fat content increases thermal

resistance so that even considerable heating is required to

eliminate Salmonella and (iii) a small number of Salmo-nella can cause illness (11 129)

In honey which may be consumed as is or used as an

ingredient in confectionary products Salmonella may

survive for over 29 weeks at 22uC (12) Halva is another

confectionary product with very low aw of 018 The product

consists of tahini (a paste of milled roasted sesame seeds)

sugar citric acid and soapwort root extract Sometimes

cocoa powder and pistachios or walnuts are mixed in with

the halva to enhance flavor Some of the ingredients (eg

sesame seeds cocoa powder nuts and flour) have the

potential to be contaminated with Salmonella Although

Salmonella cells do not multiply because of the low water

activity the organism may survive for relatively long

periods in the product Salmonella Enteritidis survived in

vacuum-packed halva stored for 8 months under refriger-

ation longer than its survival in air-sealed halva stored at

room temperature (74) The greatest decline in viable


Salmonella Enteritidis counts from an initial inoculum of

log 387 to log 215 CFUg was observed in air-sealed

packed product stored after 8 months at room temperature

The author concluded that reduction of salmonellae during

storage cannot be predicted solely on the basis of water

activity Interactions between low water activity and

environmental factors such as temperature and storage in

air or under vacuum appear to play an important role in

Salmonella survival Some examples of the survival of

Salmonella in foods of low water activity are presented in

Table 2

Peanut butter and nuts Salmonella inoculated into

peanut butter and nut spreads may aggregate or clump

within or near the water phase of the colloidal suspension of

lipid and water in the peanut meal phase If nutrient

availability is affected by cell density within water droplets

then the viability of Salmonella would be expected to differ

depending on the size of the water droplets which may vary

with the product (18 28 42 109) Viability of Salmonellain food products may also be influenced by storage

temperature level of contamination and product formula-

tion (13 18 121) For example in peanut butter and peanut

butter spread inoculated with 57 log CFUg reductions of

Salmonella in products stored for 24 weeks at 21 and 5uCwere 41- to 45-log and 29- to 43-log reduced

respectively depending on the product formulation At a

lower inoculum (15 log CFUg) six of the seven products

evaluated were positive for the pathogen at 5uC while at

21uC only one product was positive for Salmonella after

storage for 24 weeks (18) If postprocess contamination of

peanut butter and spreads occurs it may result in survival of

salmonellae in these products during their shelf life at 5uCand possibly at 21uC depending on the formulation (1828) Thermal inactivation models showed that Salmonellasurvived in peanut butter for a much longer time than

predicted (86) highlighting the danger associated with the

extrapolation of the predictive models beyond their intended

TABLE 1 Survival of Salmonella in milk chocolate and bitter chocolate at 20uCa

Storage time

Level of Salmonella (log MPN100 g)

Typhimurium Eastbourne

Milk chocolate (aw of 037) Bitter chocolate (aw of 042) Milk chocolate (aw of 038) Bitter chocolate (aw of 044)

0 504 486 52 52

1 day 234ndash263 169ndash188 464 464

13 days 118ndash136 030ndash056 254ndash318 130ndash190

20 days 089ndash111 Negndash030 254ndash297 118ndash156

34 days Negndash089b Neg NDc ND

41 days ND ND 223ndash238 065ndash118

48 days Negndash089 Neg ND ND

76 days ND ND 163ndash169 Negndash146


6 mo Neg Neg Negndash123 Neg

9 mo ND ND 089ndash111 Neg

a Adapted from Tamminga et al (117)b Neg Salmonella not detectedc ND not determined

TABLE 2 Examples of Salmonella survival in foods with low water activity

Food Salmonella serotype(s)

Inoculum

(log CFUg) aw Length of survival Reference

Dried milk products Contaminated naturally

with three serotypes

10 mo 100

Pasta Infantis Typhimurium 12 moisture 12 mo 102Milk chocolate Eastbourne 80 041 9 mo at 20uC 117

50 038 9 mo at 20uCBitter chocolate Eastbourne 70 051 9 mo at 20uC 117

50 044 76 days at 20uCHalva Enteritidis 70 018 8 mo at refrigeration temp 74Peanut butter A composite of Agona 57 020ndash033 24 wk held at 5 or 21uC 18

Enteritidis Michigan

Montevideo

Typhimurium

15 020ndash033 24 wk at 5uC6 wk at 21uC

Paprika powder Multiple serotypes 8 mo 78


range Factors including pH and fat content could account

for the differences seen between the predicted and the

experimental results In other words it is important to have

laboratory-based models with real foods since the individ-

ual properties of foods may have a great impact on the

survival of microorganisms within foods (86) Nut and seed

products may be naturally contaminated with Salmonella

due to the nature of cultivation harvesting and epidemi-

ologic history Salmonella was identified as a biological

hazard in this type of products A large number of nut and

seed products including peanuts pistachios pecans

hazelnuts and sesame and sunflower seeds have been

recalled due to Salmonella contamination A study by

Uesugi et al (121) demonstrated the potential for long-term

environmental presence or persistence of Salmonella in

almond orchards Salmonella was isolated from an almond

farm over a period of 5 years and all 53 isolates obtained

were Salmonella Enteritidis PT 30 belonging to two pulsed-

field gel electrophoresis patterns This rare Salmonella strain

was isolated in an outbreak in 2000 and 2001 that was

linked to the consumption of raw almonds (121 122) If

almond hulls and shells are wet Salmonella can grow by

using nutrients available in the almond hull andor shells

and penetrate the almond hulls into the kernels during wet

conditions such as rainfall or from other water sources

(121) Survival of Salmonella on pecans stored at different

temperatures up to 32 weeks was inversely correlated to the

storage temperature (13) Although storage for nuts and nut

products (which have a relatively high fat level) at lower

temperatures may be beneficial in preventing oxidative

rancidity lower temperatures may enhance the survival of

foodborne pathogens such as Salmonella (121)

Spray-dried milk eggs and dry yeast During the

spray drying of foods such as dairy products (whole milk

skim milk and whey) egg products (whole egg egg white

and egg yolk) and dry yeast various factors may influence

the survival of Salmonella in the final product (90) For

example 60-log reductions of Salmonella Typhimurium

were observed in concentrated skim milk with 20 total

solids in comparison with 33-log reductions in 40 total

solids at moisture levels of 37 and 30 respectively (90)Even at similar levels of moisture (6) a greater

destruction of Salmonella Typhimurium was observed in

the process of drying of 20 solids concentrate although

the processing temperature was lower than that of 40

solids The authors concluded that much less survival

occurred in the less dense product For the egg products the

greatest log reduction of 62 occurred in egg yolk (90) The

authors pointed out that whole milk and whole eggs

presented similar protection on artificially inoculated

Salmonella cells when products were dried from 40 solid

concentrates Approximately the same degree of Salmonelladeath was achieved for both skim milk (20 solids) and

concentrated yeast (25 solids) when dried under similar

conditions (90) Several interrelated factors determine to

what extent the enteric bacteria such as Salmonella and Ecoli survive the spray-drying process The most important

factors that influence the survival of Salmonella in spray-

dried products are product temperature during process

particle density fat content and strain variation (81 90)Food processors should not depend on the drying process to

replace adequate pasteurization prior to drying and they

should also be very cautious and avoid contamination

during and after drying (90) Multiple factors such as

numbers of organisms present initially serotype type of

product or processing time and temperature may influence

the survival of Salmonella in dried milk products during

storage Presence of salmonellae was detected in some

samples after 1 year of storage (100) Jung and Beuchat (66)showed that Salmonella Typhimurium survival was en-

hanced as the water activity of egg white powder decreased

The investigators detected Salmonella in the powder at an

aw of 013 but not at an aw of 034 after the product was

stored at 54uC for 7 days

Flours pasta and spices Flour is typically used as an

ingredient in more complex cooked or baked foods that

receive effective killing steps for Salmonella and other

vegetative pathogens before eaten Generally the FDA does

not consider flour a lsquolsquosensitive ingredientrsquorsquo for Salmonella(113) However there are circumstances where flour must

be pretreated to eliminate the pathogen eg when it is used

as a carrier for nutraceuticals pharmaceuticals spices and

flavors or as a bulking-caloric agent in dried mixes such as

in ready-to-eat foods for elderly people or infants (113)Rayman et al (102) were able to detect Salmonella Infantis

and Salmonella Typhimurium from pasta after 360 days of

storage demonstrating that prolonged storage of pasta is not

an effective means of decontamination for contaminated

product Spices and dried vegetable foods such as

mushrooms parsley asparagus peppermint and pepper

are occasionally contaminated with Salmonella Reports on

Salmonella outbreaks associated with the consumption of

these types of foods have been published For example as

noted previously Lehmacher et al (78) described a

Salmonella outbreak associated with the consumption of

paprika-powdered potato chips Although low levels of

Salmonella survived in the product (4 to 45 cells per 100 g)

those levels were sufficient to cause illnesses possibly

because of the high fat content of the paprika-powdered

potato chips which may have protected Salmonella from

gastric acidity

Pet treats In 1999 an outbreak of Salmonella Infantis

in Canada was linked to contact with pet treats (30) In a

survey White et al (130) reported that 41 of dog treat

samples were positive for Salmonella Raw hides used for

preparation of dog chews are expected to be contaminated

with salmonellae and if Salmonella is not controlled

adequately pet treats could be potential sources of animal

and human infections with Salmonella (27 30 97 130)

Survival of Salmonella in other matrices De

Rezende et al (36) suggested that an in vitro adaptation

of Salmonella to dry environments might occur when the

organisms are exposed to alternating levels of high and low

water activity The maximum survival of several vegetative


bacteria in dried milk was between aw values of 005 and

020 Maximum survival of Salmonella Newport in foods at

neutral pH was at an aw of 011 According to Burnett et al

(18) and Christian (28) Salmonella Senftenberg and

Salmonella Typhimurium survived in gelatin in a rubbery

state (093 to 096 aw) and a glassy state (045 to 028 aw)

Salmonella cells remained viable under low-water-activity

conditions and the lowest survival levels were observed at

an intermediate aw between 055 and 074 (29)Desiccated Salmonella cells can survive for a long time

on work surfaces and in foods with low water activity

especially in those foods with a high fat content Although

some inactivation occurs in dehydrated foods during storage

the degree depends on relative humidity and storage

atmosphere Simulating conditions in dried foods Hiramatsu

et al (60) showed that desiccated cells of different Salmonellastrains inoculated on dried paper disks were inactivated after

35 to 70 days of storage at 25 and 35uC but the cells survived

22 to 24 months when stored at 4uC The investigators

concluded that preserving dry foods contaminated with

Salmonella and stored at refrigerated temperatures might

present a higher food safety risk Flowers (44) reported that

the higher water activity storage temperatures and oxygen

levels the higher the death rates of Salmonella

Recovery of Salmonella stressed by low-moistureenvironments While there are several relatively straight-

forward methods for recovery of uninjured bacterial cells

the same cannot be said about sublethally injured cells

surviving a processing treatment More sensitive methods

for recovery of the injured Salmonella cells especially from

low-moisture or desiccated foods are needed Factors

including the elimination of oxygen gradual rehydration

enrichment broth plating media incubation time and

temperature and the addition of solutes (ie glycerol

glucose) may contribute to a better recovery of the cells

injured by heat or desiccation (47 50 70 86 88 101 133)The recovery of the injured cells by heating at a water

activity is improved by gradual rehydration especially when

using isotonic dilution media prolonged incubation and

agents to protect against reactive oxygen A rapid and large

increase in water activity during the rehydration may result

in cellular lysis which will trigger an inaccurate estimation

of the survivors The use of solutions containing glycerol

lactose sucrose or milk solids to rehydrate the freeze-dried

Salmonella resulted in higher recoveries than when the

water was used for rehydration (86 88 101) Although slow

rehydration of cells was found to be beneficial in some dried

foods it may not hold true for all food products The

dehydration procedure should be validated on each

individual food basis (33) Mattick et al (86) considered

that gradual rehydration might have also an important

contribution in accurate determination of the infectious dose

for Salmonella associated with low-moisture food implicat-

ed in a food outbreak

Mechanisms for Salmonella survival Salmonellamay enter a viable but nonculturable (VBNC) state which

represents a dormant state of the vegetative cells and a

survival strategy for many nonsporulating species (21 79)De Rezende et al (36) also showed extensive filamentation

of Salmonella Typhimurium DT104 cells after exposure to

low water activity Gupte et al (54) succeeded in

resuscitating the nonculturable organism by temperature

increase and nutrient addition and confirmed the develop-

ment of the VBNC state for Salmonella Typhimurium

DT104 The investigators suggested that entering a VBNC

state might enable the organism to maintain viability in

inimical conditions and revert to the normal state under

favorable conditions It is not clear however whether

Salmonella in a VBNC state maintains its pathogenic

capacity and therefore is a concern for food safety (21 79131) Several research groups have demonstrated the

capacity of other bacteria (such as enteropathogenic E coliVibrio vulnificus and Edwardsiella tarda) to retain their

pathogenicity in a VBNC state (38 95 98)Biofilm formation is another way by which Salmonella

survives the hostile conditions of the environment (112)However based on available literature it is not clear

whether Salmonella cells form biofilms under low-moisture

conditions

A study by Mattick et al (85) showed the presence of

Salmonella filaments after 144 h of incubation in a broth

medium supplemented with 8 NaCl (an approximate aw of

095) therefore the authors hypothesized that filamentation

may improve survival Filaments occur as a consequence of

exposure of Salmonella to marginal growth conditions such

as lower water activity high or low temperatures (including

refrigerated temperatures) and high or low pH values (6987) Kieboom et al (69) showed that reduced water

activity affected the morphology of Salmonella Enter-

itidis cells which elongated and formed filaments when

incubated at aw of 094 to 095 at 25uC for 6 days Although

cell filamentation increased the optical density of the

broth culture no increase in CFU was observed on plates

which suggests that filament cells form single colonies on

the agar

Research has also investigated other mechanisms that

may enhance Salmonella survival Abee and Wouters (2)showed that the adaptability of Salmonella Typhimurium to

osmotic stress is most efficiently mediated by the accumu-

lation of betaine (NNN-trimethyl glycine) via specific

transporters In response to increased osmotic pressure

Salmonella can modify the composition of its outer

membrane (106) Optimal growth of Salmonella Typhimur-

ium in media of high osmolarity and long-term survival

during starvation in simple solutions of different osmolarity

take place when both sE- and sS-regulated genes are

functioning The relative importance of sE and sS factors

differed depending on the environment For example at a

concentration of 6 NaCl (aw of approximately 096) sS

was more important than was sE whereas sE was more

important than was sS for survival in a solution of 085

NaCl especially at 37uC The investigators concluded that

these conditions are relevant to food preparation and

storage and sE and sS contribute toward survival of

Salmonella Typhimurium in the food chain The exposure

of Salmonella Typhimurium to conditions that activate the


sE or sS pathways could trigger enhanced survival of the

organism during food processing and storage (89) Hensel et

al (58) postulated that the water that is in close contact with

the proteins inside a bacterial cell could be a factor

determining the cellrsquos inactivation As the cell is heated

water molecules begin to vibrate and this vibration causes

the disulfide bonds and hydrogen bonds in the surrounding

proteins to weaken and break altering the final three-

dimensional configuration and possibly preventing the

protein from functioning As less water is present these

vibrations will be reduced thus decreasing protein denatur-

ation by this mechanism (39) It has been also suggested that

with reduced water in the cells the dipoles of the proteins

within the cell interact and therefore stabilize both proteins

and their subunits ie peptides and amino acids with

formation of a stable complex (118) A larger amount of

thermal energy would therefore be required to unfold the

peptide chains and the cellrsquos heat resistance would be

increased in these low moisture ranges

It is well recognized that Salmonella represents a real

hazard for a wide range of low-moisture foods and food

materials Even though the organism does not grow it may

survive for a long time and cause illness The ability of the

organism to survive under adverse environmental conditions

makes it difficult to control Unlike other gram-negative

bacterial strains (ie E cloacae E coli) Salmonella seems

to be supplied with a protection mechanism or structure that

enables this organism to survive better under desiccated

conditions (65) The mechanism by which Salmonellasurvives adverse conditions may include resistance to low

water activity biofilm formation entry into a VBNC state

and activation of genes such as the sE or sS pathways (536 54 89) However these observations largely were made

with studies conducted in a matrix with an aw above 085

The extent to which these mechanisms apply to a low-

moisture product or the dry processing environment should

be further investigated

HEAT RESISTANCE OF SALMONELLA INLOW-MOISTURE PRODUCTS

Thermal resistance of Salmonella is greatly enhanced in

low-moisture foods and may be affected by other intrinsic

and extrinsic properties of a food For this reason when

evaluating published results of heat resistance of Salmonellain a particular food one should be aware that it might be

more meaningful to compare results within a study using

similar food types and methods to determine heat resistance

than to compare results from different studies Due to

variations in these parameters it is important when using

published D- and z-values or other inactivation models and

applying them to certain food processes that the conditions

under which the values were obtained should not be

significantly different from the product or process param-

eters used by the processor Examples of published data on

the heat resistance of Salmonella spp in reduced-moisture

food products such as chocolate peanut butter almonds

cereal grain flours and spray dried milk are summarized

here

Chocolate and syrups Chocolate and chocolate

candies have such low-moisture content (aw of 04 to 05)

that organisms heated in it are essentially subjected to dry

heat Increasing the amount of cocoa in the suspending

medium as well as agitation of the suspension before

inoculation and heat treatment enhanced the lethal effect on

Salmonella (19) Several studies on the heat resistance of

Salmonella in chocolate were conducted (Table 3) to assess

the potential for the application of a heat process to

eliminate the pathogen (9 49 76) A study conducted by

Goepfert and Biggie (49) showed that in molten chocolate

Salmonella Typhimurium had a D-value of 396 min (66 h)

and 816 min (136 h) at 711 and 656uC respectively

Similar heat resistance was observed for milk chocolate

(76) in which the D-values were 45 46 and 66 h at 71uCfor Salmonella Eastbourne Salmonella Senftenberg and

Salmonella Typhimurium respectively Results from these

two studies (49 76) demonstrated that Salmonella Typhi-

murium was more heat resistant than was SalmonellaSenftenberg 775W in milk chocolate The curves obtained

in the Goepfert and Biggie (49) study showed a rapid

decline in numbers of survivors (3-log cycles) during the

first few minutes of heating followed by a slower rate of

decrease thereafter The rapid initial loss might be attributed

to the death of cells injured during the lyophilization and

inoculation methods used in this study Salmonella cells

were much more susceptible to destruction by heat when

traces of water were added to the chocolate mass Barrile

and Cone (8) studied the effect of added moisture on the D-values of Salmonella Anatum in milk chocolate at 71uC A

dramatic decrease in the D-value was evidenced with 20

added moisture reducing the D-values from 20 h to 4 h D-values decreased as the level of added moisture increased

However the change per increment of moisture was

especially pronounced at or below 20 moisture level

D- and z-values for different Salmonella serotypes in

chocolate are presented in Table 3

Sumner et al (116) determined the heat resistance of

Salmonella Typhimurium in sucrose solutions with aw

ranging from 098 to 083 The temperature data collected

were analyzed with the general method (115) used to

establish cumulative lethality for each heating time interval

The calculated lethality value was then used to determine

the decimal reduction time (D) The D656uC was 029 at an

aw of 098 and 402 min at an aw of 083 Authors also

compared data collected in the sucrose solution to data

generated using a food product two thermal death time

experiments were conducted with each of four chocolate

syrups (A B C and D) with aw values of 083 084 075

and 083 respectively At an aw of 083 and temperature of

656uC Salmonella Typhimurium was approximately three

times more heat resistant in syrup D than in syrup A The D-

values for syrups A and D were 12 and 32 min

respectively This observation was thought related to

differences in compositions of the syrups particularly

sweeteners D-values in chocolate syrups were more than

10-fold lower when compared with those in sucrose

solutions at the same aw values For examples at an aw of

083 and temperature of 656uC D-values were 32 and


402 min for chocolate syrup (pH 535) and sucrose

solutions respectively (116)In one of the first research publications dealing with the

heat resistance of Salmonella in a low-water-activity

environment Goepfert et al (50) examined the effect of

various sugar and sugar-alcohol solutions on heat resistance

by using several serotypes of Salmonella They found that

heat resistance was much greater when sucrose was used to

lower the water activity than when fructose glycerol or

sorbitol was used Salmonella Senftenberg 775W showed

less of an increase in heat resistance than did the other

strains of Salmonella as the environment became drier

Growth in a reduced-water-activity environment prior to

inoculation increased the heat resistance of Salmonella in

glycerol solutions but not in sucrose solutions The novel

conclusion of the early research was that although heat

resistance did increase at lower aw values other factors such

as the substance used to reduce the aw values had a

significant effect Therefore it is not possible to take the

heat resistance of an organism at a certain aw value in one

food type and apply it to another

Peanut butter Shachar and Yaron (109) investigated

the heat resistance of Salmonella serovars Agona Enter-

itidis and Typhimurium in peanut butter The peanut butter

was inoculated with the Salmonella serovars at 4 and 8 log

CFUg and incubated in water baths at 70 80 or 90uC for 5

to 50 min at each of the temperatures All Salmonellaserovars tested regardless of their initial cell concentration

showed no significant differences (P 005) in heat

resistance All serovars were so heat resistant that even after

50 min at 90uC only a 32-log reduction was observed

When peanut butter containing viable Salmonella cells of

serotype Agona Enteritidis and Typhimurium at approxi-

mately 8 log CFUg was exposed to heat for 5 min a 14-log

reduction was observed at 70uC a 22-log reduction at

80uC and a 25-log reduction at 90uC (109) It was

observed that after an initial inactivation phase cell death

occurred at a slower rate During the second inactivation

phase higher temperatures (80 and 90uC) were only slightly

more effective in killing cells than was 70uC but the

differences were not statistically significant at heating

intervals up to 50 min The thermal inactivation curves

were upwardly concave indicating rapid death at the

beginning (10 min) followed by lower destruction rates

and an asymptotic tail The authors applied the nonlinear

Weibull model to describe the heat inactivation of

Salmonella in peanut butter This model predicted that

more than 260 min (4 h) would be needed to reduce

Salmonella by 7 log units at 70uC and more than 1 h would

be needed at 90uC Shachar and Yaron (109) concluded that

some thermal treatments currently used in the industry to

pasteurize peanut butter (eg 70uC for 20 min) are not

sufficient to destroy vegetative cells of Salmonella The

authors concluded that a heat process of more than 4 h at

70uC or 1 h at 90uC would be adequate to deliver a 7-log

reduction but these processes may not have a practical

application because they may adversely affect the sensory

and quality properties of the product Ma et al (84) reported

nonlinear inactivation of three outbreak strains of Salmo-nella Tennessee in peanut butter and used the Weibull

model to fit the inactivation data The resistance of

Salmonella Tennessee strains was compared with the rates

of inactivation of Salmonella strains of other serotypes

(Enteritidis Typhimurium and Heidelberg) The authors

found that 41 iexcl 3 min at 90uC achieved a 5-log reduction

TABLE 3 Heat resistance of Salmonella in chocolatea

Salmonella serotype Heating medium

D-values (min) at temp indicated

z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)

Senftenberg Molten chocolate 440b 116b 36b 180 (324)b

Molten chocolate 276c

Typhimurium Molten chocolate 816b 222b 75b 190 (342)b


Chocolate syrup (A) (pH 510 aw ~ 083) 12d 62 (112)d

Chocolate syrup (B) (pH 510 aw ~ 084) 26d 76 (137)d

Chocolate syrup (C) (pH 565 aw ~ 075) 27d 83 (150)d

Chocolate syrup (D) (pH 535 aw ~ 083) 32d 77 (139)d

Anatum Molten chocolate (no moisture added) 1200e

Molten chocolate (1 moisture added) 510e


Milk chocolate 11 242 (436)e

a Adapted in part from Doyle and Mazzotta (37)b Goepfert and Biggie (49) Cells were grown to stationary phase and then inoculated into melted chocolate Surviving cells were estimated

by the most probable number after suspension in nutrient broth and incubation at 37uC for 48 h The average D-values from three

experiments are shownc Lee et al (76)d Sumner et al (116) Cells were grown to stationary phase in brain heart infusion broth and then inoculated into chocolate syrup Surviving

cells were recovered in lactose broth incubated at 30uC for 48 h and plated on Hektoen enteric agare Barrile et al (9)


of a mixture of three outbreak-associated SalmonellaTennessee strains in peanut butter (26 iexcl 2 min were

needed to inactivate a composite of other Salmonellaisolates) Results of this study indicated that the outbreak

associated with Salmonella strains were more thermotoler-

ant than were the other Salmonella strains tested and this

greater thermal resistance was not serotype specific

Thermal treatments of 90uC for less than 30 min are not

sufficient to kill large populations (5 log CFUg) of

Salmonella in highly contaminated peanut butter

Shachar and Yaron (109) also studied the factors that

affect the high heat resistance of Salmonella in peanut

butter They suggested that the combination of both high fat

content (55) and low aw (02 to 033) in peanut butter

had a protective effect on Salmonella The authors also

explained the higher heat resistance of Salmonella in peanut

butter was based on the heterogeneous nature of the product

Since peanut butter is a highly concentrated colloidal

suspension of lipid and water in a peanut-meal phase the

bacterial cells would be exposed to different local

environments and could aggregate near the water phases

During the heat process cells would die off at different

rates depending on the protective effect of the local

environment

Almonds Traditional roasting of almonds involves

using high temperature or a long roasting time Commercial

oil roasting of almonds is carried at temperatures higher than

260uF (1267uC) and for longer than 20 min This process

is more than sufficient to yield a 5-log destruction of

Salmonella in almonds (4) If there is a need for a shorter

process process parameters for a 4-log reduction are 16 min

at a minimum oil temperature of 260uF (3 4)Abd et al (1) evaluated the impact of prior storage

temperature (4 and 23uC) on thermal inactivation at 121uC(250uF) of Salmonella Enteritidis PT30 on oil roasted

almonds Reductions of 4 or 5 log were consistently

achieved after heating for 058 iexcl 008 or 118 iexcl 017 min

respectively when almonds were stored at 4uC In contrast

at 23uC 4- or 5-log reductions were achieved after heating

for 116 iexcl 036 and 206 iexcl 057 min

New pasteurization techniques such as steam pasteur-

ization and combined hot-air roasting and pasteurization

process have been proposed for raw and roasted almonds

(96) Both processes are designated to produce a boundary

layer of humidity on the almond surface to maximal

microbiological inactivation rates The original product

quality of the almonds are maintained and not impaired

since the temporary increase in moisture content is very

little (96)Lee et al (77) studied the application of pasteurization

treatment for the reduction of Salmonella Enteritidis on an

almond surface Two varieties of California raw shelled

almonds (Nonpareil and Mission) were inoculated with

Salmonella Enteritidis and treated with steam at 93uC for 5

15 25 35 45 55 or 65 s A higher D-value (1613 s) was

calculated for Salmonella Enteritidis Mission almonds than

for the Nonpareil variety (1222 s) The data suggested that

steam treatments of 61- and 81-s durations would be

required to achieve 5-log reductions in Nonpareil and

Mission almonds respectively (77)

Spray-dried milk An increase in bacterial resistance

as solute concentration of the heating medium increases (735 92) has been reported in several publications It has been

suggested that this increase in resistance is a consequence of

reduced water activity Dega et al (35) conducted research

on the influence of milk solids concentrate at 10 30 42 and

51 (wtwt) on the thermal resistance of SalmonellaTyphimurium and Salmonella Alachua grown in tryptic

soy broth at 37uC The study showed that increasing the

solids level resulted in an increase in resistance to heat of

both strains of Salmonella In addition Salmonella Alachua

was more heat resistant in milk containing 10 30 42 and

51 solids than was Salmonella Typhimurium (Table 4)

The researchers also observed that the z-value increased as

the solids level in milk increased For examples SalmonellaAlachua z-values were reported as 41 62 and 69uC at 10

42 and 51 solids respectively The authors also

demonstrated that the growth of Salmonella Typhimurium

in 42 milk solids for 24 h did not greatly enhance the

thermal resistance of the organism when milk solutions were

heated at atmospheric pressure to obtain 42 solids

concentrate (35)McDonough and Hargrove (88) observed that a cocktail

of Salmonella (Salmonella Senftenberg Salmonella Typhi-

murium and Salmonella New Brunswick) was extremely

resistant to destruction by dry heat in non-fat dried milk

powder (Table 5) Neither 60 nor 766uC destroyed

Salmonella cells starting with an initial population of 104

CFUg after 10 h (10-g samples) The moisture level in milk

powder significantly influenced the heat resistance of

Salmonella For example 2 h was insufficient to kill

Salmonella in 4 and 7 moisture powders at 85uC

although 30 min was sufficient at the 25 moisture level

The degree of heat required for destruction at a high

temperature (1155uC for 1 h) at 4 moisture was too

intense and imparted a yellow burned appearance to the

milk powder Salmonella was not detected in milk powders

containing 15 moisture treated at 1488uC for 6 min It

was concluded that if the moisture content of milk powder

was greater than 15 milk powder might form larger

agglomerates slowing the rate of heat conductance (88)

Cereal grain flours Sperber et al (113) reported that

the incidence of Salmonella in wheat flour ranged from 014

to 132 Flour is typically an ingredient in food that is to

be cooked or further processed before consumption If there

is a possibility that the flour will be consumed without

further processing (even if that is not the intended use of the

food product) then use of flour that has been heat treated to

eliminate Salmonella may be desirable Archer et al (6)reported that the D-values for Salmonella Weltevreden in

flour ranged from a D-value of 875 min at 60 to 62uC and

an initial aW of 04 to a D-value of 29 min at 63 to 65uC and

at an initial aw of 05 (Table 6) The z-values obtained in

flour ranged from 152 to 539uC for Salmonella Weltevre-

den in wheat flour and they were considerably larger than


those values obtained in moist environments (where a

typical z-value would be 57uC) for Salmonella serotypes

(119) It was found that the lower the initial aw value of the

sample prior to heating the higher the heat resistance of the

cells They observed that the death kinetics were biphasic

with an approximately 1-log reduction in the first 5 to 10 min

of heating followed by a slower linear decrease in

survivors The investigators calculated the D-value based

on the linear portion of the survivor curve This study also

suggested that it is the initial aw value before heating not the

aw value during heating of the inoculated product that is the

significant parameter affecting heat resistance Van Cau-

wenberge et al (126) investigated the use of dry heat to

inactivate a number of Salmonella serotypes including

Newington Typhimurium Anatum Kentucky Cubana

Senftenberg Thompson and Tennessee in corn flour at

10 and 15 moisture (Table 6) The flour was spray

inoculated at 105 CFUg and then treated with dry heat at

49uC (120uF) After 24 h at either 10 or 15 moisture level

999 of the Salmonella cells (serotypes Newington

Typhimurium Anatum and Kentucky) were inactivated

A product moisture level of 15 was slightly more effective

than was a 10 moisture level in reducing the cell

population from 105 to103 CFUg Salmonella Thompson

and Salmonella Tennessee were more resistant to heat

inactivation than were the other serotypes The investigators

suggested that the incidence of Salmonella contamination in

corn flour could be significantly reduced with a heat

treatment of 49uC for 24 h (126)

Dry animal feeds Animal feeds are frequently

contaminated with Salmonella (20 82 111) Liu et al

(82) determined the thermal resistance of SalmonellaSenftenberg 775W in dry animal feeds (artificially contam-

inated and simulated naturally contaminated) at various

moistures levels Increasing feed moisture levels decreased

heat resistance with a declining effect starting between 15

and 20 moisture Data obtained from thermal death time

tubes indicated that except for initial fast killing rates the

heat resistance of Salmonella Senftenberg 775W in dry

feeds was an exponential function of heating time Heat

resistance was higher with contamination by the simulated

natural method than by broth cultures The simulated

naturally contaminated feedstuffs were prepared by inocu-

lation of Salmonella Senftenberg 775W into a sterile

suspension of meat and bone meal in distilled water

whereas artificially contaminated feedstuff was prepared by

adding a tryptic soy broth culture to feed The D-value at

140uF in simulated naturally contaminated feed was 28 min

at a 5 moisture level and was approximately 29 275

379 103 and 258 times as much at respective moisture

levels of 10 15 20 25 and 30 The z-values were in the

range of 18 to 20uF (100 to 111uC) (82)

TABLE 4 Influence of milk solids concentration on the heat resistance of Salmonella Typhimurium and Salmonella Alachua grown inTrypticase soy broth at 37uCa

Salmonella serotype

10 solids 30 solids 42 solids 51 solids

Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380

a Adapted in part from Dega et al (35)b Temperature values iexcl02uCc D-value decimal reduction time it represents an average of two to five trials at each temperature

TABLE 5 Survival of Salmonella in non-fat dried milk subjectedto dry heata

Exposure

time

Salmonella count (CFU) at temp indicated

60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1

a Adapted from McDonough and Hargrove (88) A thin layer of

conventional (4 moisture) powder was heated in an oven

Negative results from 10-g samples recorded as 1b ND not determined


Bucher et al (17) studied the thermal resistance of

Salmonella strains isolated from raw frozen chicken

nuggetsstrips nugget meat and pelleted broiler feed to

determine whether they exhibited enhanced thermal resis-

tance Salmonella Enteritidis and Salmonella Orion were

isolated from pelleted broiler feed For Salmonella Enter-

itidis D-values ranged from 693 to 015 min at 55 and

62uC respectively and the z-values from 410 to 517uC

For Salmonella Orion D-values ranged from 358 to

018 min at 55 and 62uC respectively with a z-value of

517uC Results of this study indicated that SalmonellaEnteritidis and Salmonella Orion strains did not exhibit

unusually high thermal resistance and that normal heating

(71uC) prior to consumption should eliminate these

organisms from chicken nuggetsstrips (17)

Application of published heat resistance data forestablishing lethal processes in low-moisture foods It is

highly recommended that food processors determine the

heat resistance of Salmonella in their specific low-moisture

product(s) rather than directly apply published D- and z-

values from the literature in establishing a lethal process

Published values obtained from the same or similar type

food products heating temperatures and aw values can

serve as guidance in making conservative assumptions

about sampling times at various heating temperatures As

can be seen throughout this review of heat resistance data

product composition can have an equal or greater affect than

just the water activity value on the destruction of

Salmonella The specific serotype of Salmonella used in a

new study as well the method used to recover surviving cells

can also have a significant impact on the heat resistance

values For these reasons it important that processors

understand the thermal death kinetics of Salmonella in their

specific products rather than relying solely on published

values from similar products when validating a thermal

process

CONCLUSION

Salmonella is extensively populated throughout nature

and can be associated with many foods in part because the

organism can inhabit a multiplicity of hosts (11) Accord-

ingly to prevent the ingress of Salmonella into the factory

prudent processors should identify both food and non-food

sources of the organism and either reject or securely isolate

these sources whenever possible When the production of a

given product involves the receipt and handling of known

sources of Salmonella such as for processors of raw

agricultural commodities establishments should have con-

TABLE 6 Heat resistance of Salmonella in cereal influenced by water activity

Salmonella serotype Heating medium aw (min) Temp (uC) D-value (min) z-value (uC) Reference

Weltevreden Wheat flour 050ndash060 69ndash71 80 303 672ndash74 45

75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77

035ndash040 69ndash71 152

72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152

63ndash65 66ndash68 80ndash100

05 63ndash65 29 539

Newington Dry corn flour Not reporteda 49 18 Not reported 126Typhimurium 48

Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264

Senftenberg (10) 366

Tennessee 594

a Moisture content was 15 unless otherwise indicated in parentheses next to the serotype


trol measures to mitigate the risks associated with handling

these potential sources These include minimizing vectors

for the transfer of Salmonella to other locations throughout

the facility by utilizing programs such as proper storage

practices balance of air flow preventive maintenance

control of employee traffic patterns and other GMPs

Additional efforts should be made to prevent the organism

from becoming embedded or otherwise well-established in

the factory environment such as sanitary design of the

facility and processing equipment effective sanitation

practices and preventing the introduction of moisture into

normally dry environments

Due to the ability of Salmonella to adapt to the stresses

of extreme physical and chemical conditions such as

desiccation temperature pH lack of nutrients etc it may

persist for a long time in dry environments Even though the

organism does not grow in low-moisture food products such

as dry milk powder chocolate or peanut butter and almonds

(11 18 121 132) it can remain viable for extended periods

especially when stored at refrigeration temperature Ac-

cordingly Salmonella spp represent a potential severe


materials if not controlled


low-moisture foods Given the fact that the heat resistance

of Salmonella is affected by many factors comparing heat

resistance among studies can be misleading Comparing

differences in heat resistance from experiments within the

same study is more accurate than is comparing data from

different experiments or studies using different conditions

Due to variations in these parameters it is important when

using published D- and z-values or other inactivation

models and applying them to certain food processes that

the conditions under which the values were obtained should

not be significantly different from the product or process

parameters used by the processor Survivor curves of heat

inactivation of Salmonella can be nonlinear and may have a

significantly asymptotic tailing effect which can affect the

efficacy of some processes Often nonlinear models

particularly the Weibull model have been used to describe

more accurately the thermal resistance of Salmonella in a

variety of low-moisture foods when compared with

traditional log-linear techniques Therefore expert microbi-

ologists and thermal process authorities with low-water-

activity food experience should be consulted for determin-

ing the appropriate thermal process for these food products

The attributes mentioned in our review characterize a

low-moisture food processorrsquos challenges a widespread

highly adaptive organism with considerable heat resistance

under low-moisture conditions Low-moisture food proces-

sors would be well advised to enact a multitude of highly

disciplined control measures to address the organism and

combat it to the fullest In 2008 in response to the

Salmonella outbreaks in low-moisture foods issues the

Grocery Manufacturers Association formed a join Salmo-nella Control Task Force to develop industry guidance

Scientific data and information summarized in this review

were used in part to develop those guidance documents (2526 52 108)

ACKNOWLEDGMENTS

The authors gratefully acknowledge the valuable assistance of

Virginia N Scott (GMA currently with FDA) Yuhuan Chen (GMA)

and Ai Kataoka (GMA)

REFERENCES

1 Abd S J K L McCarthy and L J Harris 2008 Use of the

Weibull model to evaluate the impact of storage time and

temperature on thermal inactivation of Salmonella Enteritidis PT

30 on oil-roasted almonds P1-33 IAFP 2008 Abstract Book IAFP

annual meeting Columbus OH 3 to 6 August

2 Abee T and J A Wouters 1999 Microbial stress response in

minimal processing Int J Food Microbiol 5065ndash91

3 Almond Board of California 2007 Processing authority kit

4 Almond Board of California 2007 Guidelines for validation of oil

roasting processes v 10 index VG003 Modesto CA

5 Anriany Y A R M Weiner J A Johnson C E De Rezende and

S W Joseph 2001 Salmonella enterica serovar Typhimurium

DT104 displays a rugose phenotype Appl Environ Microbiol 67

4048ndash4056

6 Archer J E T Jervis J Bird and J E Gaze 1998 Heat resistance

of Salmonella Weltevreden in low-moisture environments J Food

Prot 61969ndash973

7 Baird-Parker A C M Boothroyd and M Jones 1970 The effect

of water activity on the heat resistance of heat sensitive and heat

resistant strains of salmonellae J Appl Bacteriol 33515ndash22

8 Barrile J C and J F Cone 1970 Effect of added moisture on the

heat resistance of Salmonella Anatum in milk chocolate Appl

Microbiol 19177ndash178

9 Barrile J C J F Cone and P G Keeney 1970 A study of

salmonellae survival in milk chocolate Manuf Confect 5034ndash39

10 Bell C and A Kyriakides 2002 Salmonellamdasha practical approach to

the organism and its control in foods Blackwell Science Malden MA

11 Betts R 2007 lsquolsquoWater water everywhere nor any drop to

drinkrsquorsquomdashThe problem of Salmonella in low-moisture foods IAFP

Special Interest Session on Salmonella growth persistence and

survival in low-moisture foods and their environmentmdashstrategies for

control 94th Annu Meet IAFP Buena Vista FL 8 to 11 July 2007

12 Beuchat L R 2009 Behavior of Salmonella in foods with low

water activity Presentation at IAFP Rapid response symposium

lsquolsquoSalmonella in peanut butter products understanding the risk and

controlling the processrsquorsquo Arlington VA 26 March 2009

13 Beuchat L R and E K Heaton 1975 Salmonella survival on

pecans as influenced by processing and storage conditions Appl

Environ Microbiol 29795ndash801

14 Booth J 21 July 2006 Cadburyrsquos chocolate caused Salmonella

outbreak Times Online Available at httpwwwtimesonlinecouk

article02-228012100html Accessed 26 May 2010

15 Breuer T 1999 CDC investigations the May 1998 outbreak of

Salmonella Agona linked to cereal Cereal Foods World 44185ndash186

16 Brockman S O I Piechotowski and P Kimmig 2004 Salmonella

in sesame seed products J Food Prot 67178ndash180

17 Bucher O J Y DrsquoAoust and R A Holley 2008 Thermal

resistance of Salmonella serovars isolated from raw frozen chicken

nuggetsndashstrips nugget meat and pelleted broiler feed Int J Food


18 Burnett S L E R Gehm W R Weissinger and L R Beuchat

2000 Survival of Salmonella in peanut butter and peanut butter

spread J Appl Microbiol 89472ndash477

19 Busta F F and M L Speck 1968 Antimicrobial effect of cocoa

on salmonellae Appl Microbiol 16424ndash425

20 Butcher G D and R D Miles 1995 Minimizing contamination in

feed mills producing poultry feed Veterinary MedicinendashLarge

Animal Clinical Sciences Department Florida Cooperative Exten-

sion Service Institute of Food and Agricultural Sciences University

of Florida Gainesville

21 Caro A P Got J Lesne S Binard and Bernard Baleux 1999

Viability and virulence of experimentally stressed nonculturable

Salmonella Typhimurium Appl Environ Microbiol 653229ndash3232


22 Centers for Disease Control and Prevention 1993 Salmonella

serotype Tennessee in powdered milk products and infant formulamdash

Canada and United States 1993 Morb Mortal Wkly Rep 42516ndash

517

23 Centers for Disease Control and Prevention 1998 Multistate

outbreak of Salmonella serotype Agona infections linked to toasted

oats cerealmdashUnited States AprilndashMay 1998 Morb Mortal Wkly

Rep 47462ndash464


outbreak of Salmonella serotype Tennessee infections associated

with peanut buttermdashUnited States 2006ndash2007 Morb Mortal Wkly

Rep 56521ndash524

25 Chen Y V N Scott T A Freier J Kuehm M Moorman J

Meyer T Morille-Hinds L Post L A Smoot S Hood J

Shebuski and J Banks 2009 Control of Salmonella in low-

moisture foods II hygiene practices to minimize Salmonella

contamination and growth Food Prot Trends 29435ndash445




moisture foods III process validation and environmental monitor-

ing Food Prot Trends 26493ndash508

27 Chiewchan N W Pakdee and S Devahastin 2007 Effect of water

activity on thermal resistance of Salmonella Krefeld in liquid

medium and on rawhide surface Int J Food Microbiol 11443ndash49

28 Christian J H B 2000 Drying and reduction of water activity pp

146ndash174 In B Lund A Baird-Parker and G M Gould (ed) The

microbiological safety and quality of food Aspen Publishers Inc

Gaithersburg MD

29 Christian J H B and B J Stewart 1973 Survival of

Staphylococcus aureus and Salmonella Newport in died foods as

influenced by water activity and oxygen p 107ndash119 In B C

Hobbs and J H B Christian (ed) The microbiological safety of

foods Academic Press London

30 Clark C J Cunningham R Ahmed D Woodward K Fonseca S

Isaacs A Ellis C Anand K Ziebell A Muckle P Sockett and F

Rodgers 2001 Characterization of Salmonella associated with pig

ear dog treats in Canada J Clin Microbiol 393962ndash3968

31 Craven P C D C Mackel W B Baine W H Barker and E J

Gangarosa 1975 International outbreak of Salmonella Eastbourne

infection traced to contaminated chocolate Lancet 1788ndash792

32 Crumrine M H V D Foltz and J O Harris 1971 Transmission

of Salmonella Montevideo in wheat by stored-product insects Appl


33 DrsquoAoust J-Y 1977 Salmonella and the chocolate industry a

review J Food Prot 40718ndash727

34 DrsquoAoust J-Y and A M Sewell 1986 Slow rehydration for

detection of Salmonella spp in feeds and feed ingredients Appl


35 Dega C A J M Goepfert and C H Amundson 1972 Heat

resistance of salmonellae in concentrated milk Appl Microbiol 23

415ndash420

36 De Rezende C L E E T Mallinson A Gupta and S W Joseph

2001 Salmonella spp are affected by different levels of water

activity in closed microcosms J Ind Microbiol Biotechnol 26

222ndash225

37 Doyle M E and A S Mazzotta 2000 Review of studies on the

thermal resistance of salmonellae J Food Prot 63779ndash795

38 Du M J Chen X Zhang A Li Y Li and Y Wang 2007

Retention of virulence in a viable but nonculturable Edwardsiella

tarda isolate Appl Environ Microbiol 731349ndash1354

39 Earnshaw R G J Appleyard and R M Hurst1995 Understand-

ing physical inactivation process combined preservation opportu-

nities using heat ultrasound and pressure Int J Food Microbiol

28197ndash219

40 Ehret E 2009 Salmonella in peanut products understanding the risk

and controlling the process Overview of a 2007 voluntary recall

GMA Rapid Response Symposium Arlington VA 23 March 2009

41 Elliot E L 2005 Salmonella Enteritidis outbreak from raw

almonds Food Saf Mag 113 24 26 28ndash32

42 European Commission 2003 Opinion of the scientific committee

on veterinary measures relating to public health on salmonellae in

foodstuffs (adopted on 14 and 15 April 2003) Available at http

eceuropaeufoodfsscscvout66_enpdf Accessed 26 May 2010

43 Evans M R J P Tromans E L S Dexter C D Ribeiro and D

Gardner 1996 Consecutive Salmonella outbreaks traced to the

same baker Epidemiol Infect 116161ndash167

44 Flowers R S 2004 Salmonella pp 3ndash6 In Bacteria associated

with foodborne diseases Institute of Food Technologists Avail-

able at httpwwwiftorgKnowledge20CenterRead20IFT

20PublicationsScience20ReportsScientific20Status20Summaries

Bacteria20Associated20with20Foodborne20Diseasesaspx

Accessed 26 May 2010

45 Foster J W and M P Spector 1995 How Salmonella survive

against the odds Ann Rev Microbiol 49145ndash74

46 Funk J 5 April 2007 Moisture led to Salmonella outbreak AP

News Available at httpwwwusatodaycomnewshealth2007-04-

05-160772288_xhtmloc~interstitialskip Accessed 26 May 2010

47 George S M L C C Richardson I E Pol and M W Peck

1998 Effect of oxygen concentration and redox potential on

recovery of sublethally heat-damaged cells of Escherichia coli

O157H7 Salmonella enteritidis and Listeria monocytogenes J

Appl Microbiol 84903ndash909

48 Gill O N P N Sockett C L Bartlett M S Vaile B Rowe R J

Gilbert C Dulake H C Murrell and S Salmaso 1983 Outbreak

of Salmonella napoli infection caused by contaminated chocolate

bars Lancet 12574ndash577

49 Goepfert J M and R A Biggie 1968 Heat resistance of

Salmonella Typhimurium and Salmonella Senftenberg 775W in

milk chocolate Appl Microbiol 161939ndash1940

50 Goepfert J M I K Iskander and C H Amundson 1970 Relation

of the heat resistance of salmonellae to the water activity of the

environment Appl Microbiol 19429ndash433

51 Greenwood M H and W L Hooper 1983 Chocolate bars

contaminated with Salmonella napoli an infectivity study Brit

Med J 2861394

52 Grocery Manufacturers Association 2009 Control of Salmonella in

low-moisture foods Available at httpwwwgmaonlineorgscience

SalmonellaControlGuidancepdf Accessed 26 May 2010

53 Grocery Manufacturers Association 2010 Equipment design check-

list for low moisture foods Available at httpwwwgmaonline

orgscienceGMA_Equipment_Design_Checklist_January2010xls


54 Gupte A R C L E de Rezende and S W Joseph 2003

Induction and resuscitation of viable but nonculturable Salmonella

enterica serovar Typhimurium DT104 Appl Environ Microbiol

696669ndash6675

55 Hall P 2008 Salmonella in sesame seed products Recontamination

issue in the food processing industry what where and how

important are they IAFP Latin America Symposium on Food

Safety Campinas Sao Paulo Brazil 26 to 28 May 2008

56 Harris L J 2008 Salmonellamdashfactors affecting resistance to heat

International Association for Food Protection Symposium S8mdash

Validating processes for reducing Salmonella in low water activity

foods IAFP annual meeting Columbus OH 3 to 6 August 2008

57 Hedberg C W J A Korlath J-Y DrsquoAoust K E White W L

Schell M R Miller D N Cameron K L MacDonald and M T

Osterholm 1992 A multistate outbreak of Salmonella Javiana and

Salmonella Oranienburg infections due to consumption of contam-

inated cheese JAMA 223204ndash3208

58 Hensel H K Bruck and P Raths 1973 Homeothermic

organisms p 503ndash761 In H Precht J Christophersen H Hensel

and W Larcher (ed) Temperature and life Springer New York

59 Hills B P C E Manning Y Ridge and T Brocklehurst 1997

Water availability and the survival of Salmonella typhimurium in

porous systems Int J Food Microbiol 36187ndash98

60 Hiramatsu R M Matsumoto K Sakae and Y Miyazaki 2005

Ability of Shiga toxinndashproducing Escherichia coli and Salmonella

spp to survive in a desiccation model system and in dry foods Appl



61 Hockin J C J-Y DrsquoAoust D Bowering J H Jessop B Khanna

H Lior and M E Milling 1989 An international outbreak of

Salmonella Nima from imported chocolate J Food Prot 5251ndash54

62 Horner K J and G D Anagnostopoulos 1972 Viability of

Staphylococcus aureus Salmonella Typhimurium and Salmonella

Senftenberg heated and recovered on a solid medium of controlled

water activity J Sci Food Agric 23543ndash544

63 International Commission on Microbiological Specifications for

Foods 2005 Cereals and cereal products section IV flour starches

and meals p 409ndash413 Nuts oilseeds and dried legumes section

VI legume products p 460ndash461 In Microorganisms in foods 6

microbial ecology of food commodities 2nd ed Kluwer Academic

Plenum Publishers New York

64 Isaacs S J Aramini B Ceibin J A Farrar R Ahmed D

Middleton A U Chandran L J Harris M Howes E Chan A S

Pichette K Campbell A Gupta L Y Lior M Pearce C Clark F

Rodgers F Jamieson I Brophy and A Ellis 2005 An

international outbreak of salmonellosis associated with raw almonds

contaminated with a rare phage type of Salmonella Enteritidis J

Food Prot 68191ndash198

65 Janning B P H inrsquot Veld S Notermans and J Kramer 1994

Resistance of bacterial strains to dry conditions use of anhydrous silica

gel in a desiccation model system J Appl Bacteriol 77319ndash324

66 Jung Y S and L R Beuchat 1999 Survival of multidrug-resistant

Salmonella typhimurium DT104 in egg powders as affected by

water activity and temperature Int J Food Microbiol 491ndash8

67 Juven B J N A Cox J S Bailey J E Thomson O W Charles

and J V Shutze 1984 Survival of Salmonella in dry food and feed

J Food Prot 47445ndash448

68 Kapperud G J Lassen K Dommarsnes B E Kristiansen D A

Caugant E Ask and M Jahkola 1990 Outbreak of Salmonella

typhimurium infection traced to contaminated chocolate and caused

by a strain lacking the 60-megadalton virulence plasmid J Clin


69 Kieboom J K D Harshi M H Tempelaars W C Hazeleger T

Abee and R R Beumer 2006 Survival elongation and elevated

tolerance of Salmonella enterica serovar Enteritidis at reduced water

activity J Food Prot 692681ndash2686

70 Kirby R M and R Davies 1990 Survival of dehydrated cells of

Salmonella typhimurium LT2 at high temperatures J Appl

Bacteriol 68241ndash246

71 Kirk M D C L Little M Lem M Fyre D Genobile A Tan J

Threlfall A Paccagnella D Lightfoot H Lyi L McIntyre L

Ward D J Brown S Surnam and I S Fisher 2004 An outbreak

due to peanuts in their shell caused by Salmonella enterica serotypes

Stanley and Newportmdashsharing molecular information to solve

international outbreaks Epidemiol Infect 132571ndash577

72 Koch J A Schrauder K Alpers D Werber C Frank R Prager W

Rabsch S Broll F Feil P Roggentin J Bockemuhl H Tschape A

Ammon and K Stark 2005 Salmonella Agona outbreak from

contaminated aniseed Germany Emerg Infect Dis 111124ndash1128

73 Kopanic R J B W Sheldon and C G Wright 1994

Cockroaches as vectors of Salmonella laboratory and field trials


74 Kotzekidou P 1998 Microbial stability and fate of Salmonella

Enteritidis in halva a low-moisture confection J Food Prot 61

181ndash185

75 Kusumaningrum H D G Riboldi W C Hazeleger and R R

Beumer 2003 Survival of foodborne pathogens on stainless steel

surfaces and cross-contamination to foods Int J Food Microbiol

85227ndash236

76 Lee B S Kermasha and B E Baker 1989 Thermal ultrasonic

and ultraviolet inactivation of Salmonella in thin films of aqueous

media and chocolate Food Microbiol 6143ndash152

77 Lee S Y S W Oh H J Chung J I Reyes-De-Corcuera J R

Powers and D H Kang 2006 Reduction of Salmonella enterica

serovar Enteritidis on the surface of raw shelled almonds by

exposure to steam J Food Prot 69591ndash595

78 Lehmacher A J Bockemuhl and S Aleksic 1995 Nationwide

outbreak of human salmonellosis in Germany due to contaminated

paprika and paprika-powdered potato chips Epidemiol Infect 115

501ndash511

79 Lesne J S Berthet S Binard A Rouxel and F Humbert 2000

Changes in culturability and virulence of Salmonella typhimurium

during long-term starvation under desiccating conditions Int J

Food Microbiol 60195ndash203

80 Lewis D A R Paramathasan D G White L S Neil A C

Tanner S D Hill J C Bruce J M Stuart A M Ridley and E J

Threlfall 1996 Marshmallows cause an outbreak of infection with

Salmonella Enteritidis phage type 4 Commun Dis Rep CDR Rev

6R183ndashR186

81 Li Cari J and N Potter 1970 Salmonella survival during spray

drying and subsequent handling of skim milk powder III Effect of

storage temperature on Salmonella and dried milk properties J

Dairy Sci 53876ndash882

82 Liu T S G H Snoeyenbos and V L Carlson 1969 Thermal

resistance of Salmonella Senftenberg 775W in dry animal feeds

Avian Dis 13611ndash631

83 Lund B M and T Eklund 2000 Control of pH and use of organic

acids p 175ndash199 In B M Lund T C Baird-Parker and G W

Gould (ed) Microbiological safety and quality of food Aspen

Publishers Gaithersburg MD

84 Ma L G Zhang P Gerner-Smidt Y Mantripragada I Ezeoke

and M P Doyle 2009 Thermal inactivation of Salmonella in

peanut butter J Food Prot 81596ndash1601

85 Mattick K L F Joslashrgensen J D Legan M B Cole J Porter H

M Lappin-Scott and T J Humphrey 2000 Survival and

filamentation of Salmonella enterica serovar Enteritidis PT4 and

Salmonella enterica serovar Typhimurium DT104 at low water

activity Appl Environ Microbiol 661274ndash1279

86 Mattick K L F Jorgensen P Wang J Pound M H Vandeven

L R Ward J D Legan H M Lappin-Scott and T J Humphrey

2001 Effect of challenge temperature and solute type on heat

tolerance of Salmonella serovars at low water activity Appl

Environ Microbiol 67 4128ndash4136

87 Mattick K L R J Rowbury and T J Humphrey 2003

Morphological changes to Escherichia coli O157H7 commensal E

coli and Salmonella spp in response to marginal growth conditions

with special reference to mildly stressing temperatures Sci Prog

861031ndash13

88 McDonough F E and R E Hargrove 1968 Heat resistance of

Salmonella in dried milk J Dairy Sci 511587ndash1591

89 McMeechan A M Roberts T A Cogan F Jorgensen A

Stevenson C Lewis G Rowley and T J Humphrey 2007 Role of

the alternative sigma factors sE and sS in survival of Salmonella

enterica serovar Typhimurium during starvation refrigeration and

osmotic shock Microbiology 153263ndash269

90 Miller D L J M Goepfert and C H Amundson 1972 Survival

of salmonellae and Escherichia coli during the spray drying of

various food products J Food Sci 37828ndash831

91 Minnesota Department of Health Consumer Fact Sheet 2007

Prevent cross-contamination Available at httpwwwhealthstate

mnusfoodsafetycleanxcontaminationpdf Accessed 26 May 2010

92 Moats W A R Dabbah and V M Edwards 1971 Survival of

Salmonella Anatum heated in various media Appl Microbiol 21

476ndash481

93 Morita T H Kitazawa T Iida and S Kamata 2006 Prevention of

Salmonella cross-contamination in an oil meal manufacturing plant

J Appl Microbiol 101464ndash473

94 Ng H H G Bayne and J A Garibaldi 1969 Heat resistance of

Salmonella the uniqueness of Salmonella Senftenberg 775W Appl


95 Oliver J D and R Bockian 1995 In vivo resuscitation and

virulence towards mice of viable but nonculturable cells of Vibrio

vulnificus Appl Environ Microbiol 612620ndash2623

96 Perren R and F Escher 1997 Investigation on the hot air roasting

of nuts Manuf Confect 69591ndash595

97 Pitout J D M D Reisbig M Mulvey L Chui M Louie L

Crowe D L Church S Elsayed D Gregson R Ahmed P Tilley

and N Hanson 2003 Association between handling of pet treats


and infection with Salmonella enterica serotype Newport expressing

the AmpC b-lactamase CMY-2 J Clin Microbiol 414578ndash4582

98 Pommepuy M M Butin A Derrien M Gourmelon R R

Colwell and M Cormier 1996 Retention of enteropathogenicity by

viable but nonculturable Escherichia coli exposed to seawater and

sunlight Appl Environ Microbiol 624621ndash4626

99 Powell S and R W Atwell 1998 An evaluation of the collection

and analysis of epidemiological data for support of food safety

control systems J Food Prot 611170ndash1174

100 Ray B J J Jezeski and F F Busta 1971 Isolation of salmonellae

from naturally contaminated dried milk products II Influence of storage

time on the isolation of salmonellae J Milk Food Technol 34423ndash427


from naturally contaminated dried milk product J Milk Food

Technol 35607ndash614

102 Rayman M K J-Y DrsquoAoust B Aris C Maishment and R

Wasik 1979 Survival of microorganisms in stored pasta J Food

Prot 42330ndash334

103 Reij M W E D Den Aantrekker and ILSI Europe Risk Analysis

in Microbiology Task Force 2004 Recontamination as a source of

pathogens in processed foods Int J Food Microbiol 911ndash11

104 Rowe B D N Hutchinson R J Gilbert B H Hales N T Begg

H C Dawkins M Jacob F A Rae and M Jepson 1987

Salmonella Ealing infections associated with consumption of infant

dried milk Lancet 17900ndash903

105 Rushdy A A J M Stuart L R Ward J Bruce E J Threlfall P

Punia and J R Bailey 1998 National outbreak of Salmonella

Senftenberg associated with infant food Epidemiol Infect 120125ndash128

106 Rychlik I and P A Barrow 2005 Salmonella stress management

and its relevance to behaviour during intestinal colonisation and

infection FEMS Microbiol Rev 291021ndash1040

107 Scheil W S Cameron C Dalton C Murray and D Wilson 1998 A

South Australian Salmonella Mbandaka outbreak investigation using a

database to select controls Aust N Z J Public Health 22536ndash539

108 Scott V N Y Chen T A Freier J Kuehm M Moorman J



moisture foods I minimizing entry of Salmonella into a processing

facility Food Prot Trends 29342ndash353

109 Shachar D and S Yaron 2006 Heat tolerance of Salmonella

enterica serovars Agona Enteritidis and Typhimurium in peanut

butter J Food Prot 692687ndash91

110 Smith J P D P Daifas W El-Khry J Koukoutsis and A El-

Khry 2004 Shelf life and safety concerns of bakery products a

review Crit Rev Food Sci Nutr 4419ndash55

111 Snoeyenbos G H V L Carlson B A McKie and C F Smyser

1967 An epidemiological study of salmonellosis of chickens Avian

Dis 11653ndash667

112 Solano C B Garcıa J Valle C Berasain J-M Ghigo C Gamazo

and I Lasa 2002 Genetic analysis of Salmonella Enteritidis biofilm

formation critical role of cellulose Mol Microbiol 43793ndash808

113 Sperber W H and the North American Millersrsquo Association

Microbiology Working Group 2007 Role of microbiological

guidelines in the production and commercial use of milled cereal

grains a practical approach for the 21st century J Food Prot 70

1041ndash1053

114 Stevenson K E 2006 Introduction to hazard analysis and critical

control point systems p 1ndash4 In V N Scott and K E Stevenson

(ed) HACCP a systematic approach to food safety The Food

Products Association (currently the Grocery Manufacturers Associ-

ation) Washington DC

115 Stumbo C R 1973 Thermobacteriology in food processing 2nd

ed Academic Press New York

116 Sumner S T M Sandros M C Harmon V N Scott and D T

Bernard 1991 Heat resistance of Salmonella typhimurium and

Listeria monocytogenes in sucrose solutions of various water

activities J Food Sci 61741ndash1743

117 Tamminga S K R R Beumer E H Kampelmacher and F M

van Leusden 1976 Survival of Salmonella Eastbourne and

Salmonella Typhimurium in chocolate J Hyg 7641ndash47

118 Taneja S and F Ahmad 1994 Increased thermal stability of

proteins in the presence of amino acids Biochem J 303147ndash153

119 Thomas C T J C White and K Longree 1966 Thermal

resistance of salmonellae and staphylococci in foods ApplMicrobiol 14815ndash820

120 Todar K 2006 Todarrsquos online textbook of bacteriology University

of WisconsinndashMadison Department of Bacteriology Available at

httpwwwtextbookofbacteriologynet Accessed 26 May 2010

121 Uesugi A R M D Danyluk R E Mandrell and L J Harris 2007

Isolation of Salmonella Enteritidis phage type 30 from a single

almond orchard over a 5-year period J Food Prot 701784ndash1789

122 Uesugi A R and L J Harris 2006 Growth of SalmonellaEnteritidis phage type 30 in almond hull and shell slurries and

survival in drying almond hulls J Food Prot 69712ndash718

123 US Food and Drug Administration 4 January 1999 Records from

FDA pursuant to the Freedom of Information Act Malt-O-Meal

Company EIRs 61ndash2298 61 2 3 11 and 1698 and 713ndash15 21

98 Recall F-577ndash8

124 US Food and Drug Administration 2007 Update on tainted veggie

booty snack food Available at httpwwwfdagovNewsEvents

NewsroomPressAnnouncements2007ucm108948htm Accessed

26 May 2010

125 US Food and Drug Administration 2009 Records from

FDA pursuant to the Freedom of Information Act Peanut

Corporation of America form FDA 483 10909ndash20509

Available at httpwwwfdagovAboutFDACentersOfficesORA

ORAElectronicReadingRoomucm109818htm Accessed 26 May 2010

126 Van Cauwenberge J E R J Bothast and W F Kwolek 1981

Thermal inactivation of eight Salmonella serotypes on dry corn

flour Appl Environ Microbiol 42688ndash691

127 Wang G 2008 Surrogate selection strategy International Associ-

ation of Food Protection Symposium S8 Validating processes for

reducing Salmonella in low water activity foods 95th Annu Meet

IAFP Columbus OH 3 to 6 August 2008

128 Wan Norhana M N S E Poole H C Deeth and G A Dykes 2010

Prevalence persistence and control of Salmonella and Listeria in shrimp

and shrimp products a review Food Control 21343ndash361 Available

at httpwwwscribdcomdoc248411602010-Prevalence-Persistence-

and-Control-of-Salmonella-and-Listeria-In Accessed 26 May 2010

129 Werber D J Dreesman F Feil U van Treeck G Fell S

Ethelberg A M Hauri P Roggentin R Prager I S T Fisher S

C Behnke E Bartelt E Weise A Ellis A Siitonen Y Andersson

H Tschape M H Kramer and A Ammon 2005 International

outbreak of Salmonella Oranienburg due to German chocolate BMC

Infect Dis DOI 1011861471-2334-5-7 Available at httpwww

biomedcentralcom1471-233457 Accessed 26 May 2010

130 White D G A Datta P McDermott S Friedman S Qaiyumi S

Ayers L English S McDermott D D Wagner and S Zhao 2003

Antimicrobial susceptibility and genetic relatedness of Salmonellaserovars isolated from animal-derived dog treats in the USA J

Antimicrob Chem 52860ndash863

131 Winfield M D and E A Groisman 2003 Role of nonhost

environments in the lifestyles of Salmonella and Escherichia coliAppl Environ Microbiol 693687ndash3694

132 World Health Organization (WHO) 1995 Surveillance programme

Sixth report of WHO surveillance program for control of foodborne

infections and intoxications in Europe FAOWHO Collaborating Centre

for Research and Training in food Hygiene and Zoonoses Berlin

133 Xavier I J and S C Ingham 1997 Increased D-values for

Salmonella enteritidis following heat shock J Food Prot 60181ndash184

134 Zink D 2008 Environmental investigation and regulatory

response Salmonella Tennessee in peanut butter in the United

States 2007 International Association of Food Protection Sympo-

sium S1-2008 Foodborne disease update Salmonella in processed

foods 95th Annu Meet IAFP Columbus OH 3 to 6 August 2008


reported that the survival of dried Salmonella cells

substantially increased (up to 79 times) when sucrose

(36) was present in a desiccation model system compared

with one without sucrose Survival of Salmonella spp

inoculated in dried squid chips containing sucrose was 23 to

89 times greater than that in the dried paper disks whereas

the populations of Salmonella in dried plain squid without

sucrose were almost equal to those in the dried paper disks

(60) The authors also reported that Salmonella in the

presence of sucrose might survive for months in foods such

as chocolate peanut butter and potato chips The

combination of high fat and low water activity might have

a synergistic effect on Salmonella survival (60)The heat resistance of Salmonella in low-moisture

products is affected by many factors (37) These include

factors prior to heating (eg growth medium composition

growth phase growth temperature and stress such as heat or

acid) and factors during heating (eg acidity fat content

and addition of solutes to the matrix as well as the

Salmonella strains used) (56) Heat resistance observed in

an aqueous system is not applicable to a low-moisture

product For example a study by Ng and colleagues (94)found that Salmonella Senftenberg 775W was the most heat

resistant among 300 strains evaluated in an aqueous solution

(Salmonella Senftenberg 775W was 30-fold more resistant

than was any other strain evaluated) while this strain was

found to be less heat resistant than Salmonella Typhimur-

ium in chocolate (49) Salmonella Enteritidis PT30 the

target organism for raw almonds was implicated in an

outbreak and was found to be more resistant to dry heat than

were many of the strains evaluated on almonds (3 127)The aim of this review is to provide insights into the

sources and risk factors for contamination by Salmonella in

low-moisture products and to address the survival and heat

resistance of the pathogen with specific references that may

be used to help to develop the appropriate formulations and

processes for these products

SOURCES AND RISK FACTORS FORCONTAMINATION BY SALMONELLA IN

LOW-MOISTURE PRODUCTS

Salmonella contamination in low-moisture foods has

been traced to poor sanitation practices substandard facility

and equipment design improper maintenance poor opera-

tional practices and good manufacturing practices (GMPs)

inadequate ingredient control and other factors Many such

instances are not documented in the literature This section

summarizes and analyzes those reports that have been

published

Contamination associated with poor sanitationpractices Poor cleaning and sanitation is often cited as a

contributing factor in many outbreaks of foodborne illness

The risk of cross-contamination has been considered lower

when food contact surfaces are dry partly because bacterial

growth and survival would be reduced However Salmo-nella may be able to survive dry conditions on surfaces for

extensive time Kusumaningrum et al (75) demonstrated

that in the case of Salmonella the effects of cross-

contamination due to poor sanitation practices are enhanced

by the organismrsquos ability to survive on dry surfaces for

extended time and then transfer to foods on contact The

authors showed that Salmonella Enteritidis remains viable

on dry stainless steel surfaces and presents a potential for

contamination for considerable time Salmonella Enteritidis

was readily transferred from these test surfaces to foods

with transfer rates of 20 to 100 Salmonella Enteritidis

was recovered from dry highly contaminated (105 CFU

cm2) stainless steel surfaces for at least 4 days and for 24 h

from moderately contaminated surfaces (103 CFUcm2)

This is significant because after undertaking cleanup and

sanitation activities manufacturers typically initiate new

production much sooner than the times in these timetables

studied by Kusumaningrum et al (75) Residual concentra-

tions of organisms used in the above study should not be

found in a well-run establishment but if they are cross-

contamination potential would be high due to the transfer

rate cited here

During investigations into outbreaks of salmonellosis

evidence of Salmonella has been found in plant processing

environments (3 15 40 123ndash125) where sanitation

appeared substandard An outbreak of Salmonella Agona

associated with toasted oat cereal prompted examination of

potential cross-contamination in the processing areas air-

handling systems ingredients and traffic flow of the

manufacturing factory Investigators found widespread low

levels of the organism in the plant environment including

samples taken from the floor production equipment and the

exhaust system in the plant (15) The investigators

concluded that the unsanitary condition of the equipment

(especially the air-handling systems) poor employee

practices and poor control of the vitamin spray mixing

and holding process (eg multiple dead legs direct

connection of the vitamin supply line to the potable water

supply without maintaining proper backflow protection)

were ongoing factors with the potential to produce

contamination in the cereal product (123) An investigation

of Salmonella Senftenberg contamination in infant cereal

revealed that bulk cereal was contaminated with lsquolsquocleaning

remainsrsquorsquo from milling machinery (105) Investigations into

two consecutive Salmonella Enteritidis outbreaks in bakery

products (43) showed that the second outbreak was most

likely due to poor equipment sanitation Piping nozzles used

daily for making fresh cream cakes were inadequately

cleaned potentially allowing cross-contamination

Morita et al (93) studied the mechanisms of Salmonellacontamination in a Japanese oil meal (rapeseed or canola

meal) factory The authors found Salmonella on many

environmental vectors including operators processing area

floors dust in the air and rodents In particular high

concentrations of Salmonella were found in samples with

high oil content from the floor of the manufacturing area

The authors concluded that high Salmonella contamination

rates for the processing area represented the greatest risk for

cross-contamination of the oil meal They also stated that

restricting the movement of operators remarkably reduced

Salmonella contamination In a study involving contami-

nated chocolate by Craven et al (31) investigators






in processing mills















of the organism
























































































































































































































this risk

































































strains

























these

























































to starvation












activity itself


























































Table 2























Storage time




0 504 486 52 52

1 day 234ndash263 169ndash188 464 464













Inoculum




10 mo 100





Montevideo

Typhimurium

































































































gastric acidity



















































































conditions















the agar










































































here


























































































































z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)







































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010















































in processing mills















of the organism
























































































































































































































this risk

































































strains

























these

























































to starvation












activity itself


























































Table 2























Storage time




0 504 486 52 52

1 day 234ndash263 169ndash188 464 464













Inoculum




10 mo 100





Montevideo

Typhimurium

































































































gastric acidity



















































































conditions















the agar










































































here


























































































































z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)







































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010





































































































































































this risk

































































strains

























these

























































to starvation












activity itself


























































Table 2























Storage time




0 504 486 52 52

1 day 234ndash263 169ndash188 464 464













Inoculum




10 mo 100





Montevideo

Typhimurium

































































































gastric acidity



















































































conditions















the agar










































































here


























































































































z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)







































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010





















































this risk

































































strains

























these

























































to starvation












activity itself


























































Table 2























Storage time




0 504 486 52 52

1 day 234ndash263 169ndash188 464 464













Inoculum




10 mo 100





Montevideo

Typhimurium

































































































gastric acidity



















































































conditions















the agar










































































here


























































































































z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)







































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010
























































































to starvation












activity itself


























































Table 2























Storage time




0 504 486 52 52

1 day 234ndash263 169ndash188 464 464













Inoculum




10 mo 100





Montevideo

Typhimurium

































































































gastric acidity



















































































conditions















the agar










































































here


























































































































z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)







































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010





















































Table 2























Storage time




0 504 486 52 52

1 day 234ndash263 169ndash188 464 464













Inoculum




10 mo 100





Montevideo

Typhimurium

































































































gastric acidity



















































































conditions















the agar










































































here


























































































































z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)







































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010








































































































































gastric acidity



















































































conditions















the agar










































































here


























































































































z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)







































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010















































































































conditions















the agar










































































here


























































































































z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)







































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010































































































here


























































































































z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)







































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010












































































































z-value

in uC (uF)

656uC(150uF)

70uC(158uF)

711uC(160uF)

80uC(176uF)

90uC(194uF)







































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010
































































environment









































































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010































































































Salmonella serotype


Temp

(uC)bMean D-value

(min)cTemp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Temp

(uC)

Mean D-value

(min)

Typhimurium 571 14 580 25 608 29 650 17

557 32 550 110 596 41 628 38

525 225 517 598 588 54 623 45

514 490 585 59 610 67

570 99 570 266

551 183

Alachua 592 05 611 30 640 28

578 11 597 43 630 48

570 16 587 59 600 135

550 62 569 125 580 210

541 95 550 216 571 330

530 204 533 417 567 380



Exposure

time


60uC 766uC 850uC 1155uC

0 69 | 105 73 | 105 94 | 104 94 | 104

15 min 54 | 105 NDb ND 16 | 104

30 min 45 | 105 135 | 105 71 | 103 80 | 102

45 min ND ND ND 20 | 101

1 h 47 | 105 45 | 104 87 | 102 1

2 h 30 | 105 50 | 104 35 | 102 1

3 h 38 | 105 30 | 103 80 | 101 1

4 h ND 29 | 103 50 | 101 1

5 h 30 | 105 14 | 103 2 1

10 h 40 | 103 32 | 102 1 1






































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010












































































process

CONCLUSION














75ndash77 40ndash45

045ndash050 69ndash71 55 539

72ndash74 55

75ndash77 40ndash45

040ndash045 69ndash71 55 196

72ndash74

75ndash77


72ndash74 75

75ndash77 80

030ndash035 69ndash71 345 292

72ndash74

75ndash77 85

025ndash030 69ndash71 165 347

72ndash74 240

75ndash77 150

04 60ndash62 875 152


05 63ndash65 29 539


Kentucky 66

Anatum 48

Senftenberg 300

Cubana 150

Anatum (10) 156

Thompson 264


Tennessee 594




























































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010




































































































ACKNOWLEDGMENTS




REFERENCES














4048ndash4056



Prot 61969ndash973



















































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010














































517




Rep 47462ndash464




Rep 56521ndash524

















Gaithersburg MD























415ndash420




222ndash225









28197ndash219









































Med J 2861394











696669ndash6675

















































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010



































































































181ndash185




85227ndash236











501ndash511









6R183ndashR186





























861031ndash13
















476ndash481

































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010




























































Prot 42330ndash334






























Dis 11653ndash667








1041ndash1053


































26 May 2010











































Sources and Risk Factors for Contamination, Survival, Persistence, and Heat Resistance of Salmonella in Low-Moisture Foods

Documents