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44
Emerging Bacterial Food-Borne Pathogens
and Methods of Detection
Catherine M. Logue and Lisa K. Nolan

Introduction
Emerging Food-Borne Pathogens
Salmonella
Campylobacter
Escherichia coli Including STEC
Listeria monocytogenes

Arcobacter
Mycobacterium avium Subsp paratuberculosis
Aeromonas hydrophila
Cronobacter sakazakii (Enterobacter sakazakii)
Clostridium difficile
Antimicrobial-Resistant Pathogens
Methods for the Detection of Food-Borne Pathogens
Culture-Dependent Methods
Automated Methods to Detect Pathogens
Automated Methods of Identification
Immunologic-Based Methods of Pathogen Detection
Immunoprecipitation (Dipstick/Lateral) flow
Immunomagnetic Separation
Latex Agglutination Assays
Gel Immunodiffusion
Nucleic Acid-based Detection
Hybridization Techniques
DNA/Colony Hybridization
Polymerase Chain Reaction (PCR)
Nested PCR
Real-time PCR
Next-Generation Technologies
Adenosine Triphosphate Detection
DNA Microarrays
Immunosensors or Biosensors
Fiber Optic Biosensor
Raman and Fourier Transform Spectroscopy
Fourier Transform Infrared Spectroscopy
Surface Plasmon Resonance
Mass Sensitive Biosensors

Electronic Nose Sensors
Nanotechnology for Pathogen Detection
Summary
References

Abstract: Bacterial food-borne pathogens cause significant human
illness and misery worldwide. In this review, we focus on an examination of the bacterial pathogens associated with food-borne
illness that are common, those that are emerging and those that
are reemerging. This overview will provide the reader with an understanding of the importance of selected pathogens, the type of
disease they cause and why they should still be considered as emerging pathogens. In this review, we also focus on some of the newer
generation pathogens such as shiga toxin-producing Escherichia
coli, Arcobacter, Mycobacterium, Cronobacter, and antimicrobialresistant pathogens. The second portion of this review provides the
reader with an overview of methods for the detection of pathogens
from culture based to automated methods as well as immunologic
and nucleic acid-based techniques. Finally, this chapter includes
some overview of the next-generation technology for the detection
and characterization of pathogens including microarray, biosensor,
mass sensitive biosensors, and nanotechnology. We recognize that
the world of food-borne pathogens is ever changing and as the
pathogen poses greater challenges to the host so too does our ability
to detect and identify it in shorter timeframes.

INTRODUCTION
The costs of food-borne illnesses in terms of human health and
economic loss remain relatively unknown, but are likely to be
substantial. However, data, as it pertains to the industrialized
countries, do exist but are typically limited to a select few microorganisms; globally, the burden of food-borne illness remains
poorly understood and presents a significant challenge to society
in how to monitor and assess disease trends.
The World Health Organization seeks to respond to this data

gap by estimating the global burden of food-borne illness. In the
United States, estimates of food-borne illness have been reported
as 48 million cases, 128,000 hospitalizations, and 3000 deaths
annually (CDC 2011) placing an economic burden of US$152
billion on the nation, with an average cost of US$1850 per

Food Biochemistry and Food Processing, Second Edition. Edited by Benjamin K. Simpson, Leo M.L. Nollet, Fidel Toldr´a, Soottawat Benjakul, Gopinadhan Paliyath and Y.H. Hui.
C 2012 John Wiley & Sons, Inc. Published 2012 by John Wiley & Sons, Inc.

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illness (Schraff 2010). The Centers for Disease Control (CDC)
annual food-borne disease report posted through the FoodNet
data site reports incidences of illness based on data from ten
sentinel sites across the United States. The data cover approximately 46 million people representing approximately 15% of
the population. Current data suggest that the incidence of infections caused by Campylobacter, Salmonella, Listeria, and shiga
toxin-producing Escherichia coli (STEC), Yersinia, and Shigella
(CDC 2010) is declining.
While focusing on food-borne pathogens in this review it
is important to define what this review means by an “emerging food-borne pathogen.” Mor-Mur and Yuste (2010) suggest
that there are pathogens not previously known (new pathogens),
others that have arisen as food-borne (emerging pathogens),
and others that have become more potent with other products
(evolving pathogens). Emerging pathogens are therefore present
strains that are adapting to stresses in new environments. Emerging pathogens that have newly arisen have been recognized as a
pathogen for many years and are now associated with food-borne
transmission (Meng and Doyle 1997, 1998, Sofos 2008). While
a considerable number of pathogens are present and capable of
causing disease in foods, there are over 200 recognized natural
chemical and physical agents (Acheson 1999). Perhaps the most
important and emergent are Campylobacter jejuni, Salmonella
typhimurium DT104, E coli O157:H7, and other enterohemorrhagic E. coli (EHEC) and STEC, Listeria monocytogenes,
Arcobacter butzleri, Mycobacterium avium sbsp paratuberculosis, Aeromonas hydrophila, and Cronobacter sakazakii. Other
agents of emergence include prions, viruses, (noroviruses, hepatitis A, rotavirus), severe acute respiratory syndrome (SARS),
and parasites such as Ascaris, Cryptosporidium, and Trichinella.
Also of concern is the emergence of antibiotic-resistant strains in
pathogens such as Salmonella, Campylobacter, Shigella, Vibrio,
Staphylococcus aureus, E. coli, and Enterococci.
There are a number of factors that contribute or have had an
influence on the changing trends in food-borne disease; Newell
et al. (2010) provides an excellent overview of changes that have

occurred and contribute to the changing trends in food-borne
disease. Some of the highlights include: a rapid increase in the
human population and a shift towards an aging population; an increasing global market for foods, transportation, travel, changes
in eating habits, a greater population of immunocompromised,
and changes in farming practices and so on.
Ray (2004a) cites other factors including some which overlap
with Newell et al. (2010) that can be attributed to our recognition of how we can define an emerging food-borne pathogen.
There is an overall better knowledge of food-borne pathogens:
previously, outbreaks linked to foods were screened for a range
of standard pathogens but over the years we have expanded the
repertoire to include new pathogens. Perhaps our abilities to
test for new pathogens are based on our understanding of them.
Technologies incorporating molecular analysis and the use of
genomics have expanded our capabilities of what to search for.
So too does the technology available to rapidly screen and identify greatly expand our knowledge.
Improvements in regulations and the actions of regulatory authorities have enhanced our capabilities to rapidly identify and

monitor for emerging threats. Regulatory authorities at the state
and national levels are able to collate data regarding specific
outbreaks and the modes of transmission or vehicles implicated
in food-borne outbreaks. On the basis of this type of criteria
it is possible to make recommendations regarding criteria for
what is acceptable and what is not, as well as methods to detect
pathogens of concern. These agencies have also developed or
guide the development of appropriate sanitation procedures to
reduce the risk of human disease or educate consumers in safe
handling practices. In the United States, agencies such as United
States Department of Agriculture Food Safety and Inspection
service (USDA FSIS), and the Food and Drugs Administration
(FDA) direct some of these activities, while in Europe, the European Food Safety Authority (EFSA) has a similar role.

Changes in the lifestyle habits of consumers have changed
significantly in the last 50 years. These have included traveling,
(domestic and international), changes in consumer eating habits,
(close to half of every dollar earned is spent eating out), the
types of food consumed has changed, and there are increases
in seafood consumption, exotic foods, cheeses, and minimally
processed or more fresh or natural foods as well as greater access
to a larger variety of fresh and raw foods that are imported.
New processing technologies have led to faster and more efficient ways to produce foodstuffs for larger retail markets and
consequently there is considerably more product distributed over
a wide area—examples of the effects of this have been seen in the
outbreak of listeriosis associated with the consumption of contaminated hotdogs distributed nationally (CDC 1998, Donnelly
2001).
Some additional factors that may contribute to the emergence
of food-borne pathogens include the recognition of illness associated with multiple strains of E. coli termed STEC (Eblen
2007), or strains that appear to be emergent as a result of transfer of resistance and other genetic virulence properties (Fricke
et al. 2009), additional factors that warrant inclusion here are
also related to the transfer of antimicrobial resistance and the selection of drug-resistant strains, which can become dominant in
a food system (Endtz et al. 1991, Aarestrup and Engberg 2001,
Engberg et al. 2001, Nielsen et al. 2006, Logue et al. 2010)
and have potential links to disease that is difficult to treat. Also
of interest are the capabilities of certain pathogens to grow at
refrigeration temperatures (Listeria, Yersinia, Aeromonas) and
the ability to survive in low-pH (acid) foods (E. coli O157:H7,
Salmonella, Listeria).
In this chapter, we address emerging food-borne pathogens
of human disease and their potential impacts on human health
and methods for their detection. In general, trends in addressing
disease have shown a reduction (downward trends). The latest
data from the CDC shows prevalence in sentinel states has been

decreasing (CDC 2010).

Emerging Food-Borne Pathogens
Salmonella
Nontyphoidal Salmonella is a major cause of food-borne disease in industrialized countries. In the United States alone, it


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44 Emerging Bacterial Food-Borne Pathogens and Methods of Detection

is estimated that nontyphoidal Salmonella was responsible for
7039 illnesses per 100,000 people in 2008 (CDC 2010). The
organism colonizes a range of hosts of food animals including
poultry, cattle, and pigs and rarer animals such as bison (Li et al.
2004, Li et al. 2006, Mor-Muir and Yuste 2010). Salmonella has
also been found in a range of other habitats including soil, water,
sewage, and so on.

Salmonella outbreaks are relatively common and have been
associated with a range of foods and meats including poultry,
beef, pork, and so on. Of interest are outbreaks of illness associated with more unusual foodstuffs such as chocolate, (Werber
et al. 2005), shell eggs (Gantois et al. 2009), produce (Franz
and van Bruggen 2008), tomatoes (CDC 2005a), and peanut
butter (CDC 2009). Currently, there are over 2000 serotypes
of Salmonella recognized (Ray 2004b) and annual trends from
the CDC report common serotypes implicated in food-borne illness. The top two serotypes implicated include S. typhimurium
and Salmonella enteritidis (CDC 2010) />ncidod/dbmd/phlisdata/Salmonella.htm; some novel strains also
emerge on a regular basis.
Symptoms of human salmonellosis are usually observed as uncomplicated enteritis and enteric (typhoid) fever, which can result in a more complicated disease involving diarrhea, fever, abdominal pain, and headache. Systemic infection may also occur
resulting in a chronic reactive arthritis (Smith 1994). Salmonella
invades the mucosa of the small intestine and can proliferate in
the epithelium, and produce a toxin, which causes inflammation and fluid accumulation in the intestine. The infectious dose
required to cause illness is relatively high, about 105 –106 organisms. Most individuals develop symptoms within 24–36 hours
but the incubation time may be longer if the dose ingested is
lower. Symptoms usually last 2–3 days but patients may remain
carriers for periods of months after recovery.
Of greatest concern are S. typhimurium DT104 strains exhibiting multiple antimicrobial resistance to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline (ACSSuT), most of the resistance appears to be chromosomally encoded (Threlfall 2000). These strain types have been recognized
worldwide and have also caused infection in humans through
consumption of contaminated foods including chicken, beef,
pork sausages, and meat paste and also through occupational
contact with cattle (Wall et al. 1995, Mor-Mur and Yuste 2010).
In recent years, the incidence of S. typhimurium DT104 appears
to be declining, while resistance to other antimicrobials including extended spectrum β-lactamases appears to be increasing
(Newell et al. 2010) and have been detected in both humans and
animals (Hasman et al. 2005).

Campylobacter
Next to Salmonella, Campylobacter is the most common cause

of human food-borne disease annually in developed countries.
In the European Union, Campylobacter is the most common
cause of acute food poisoning; over 20,000 cases were reported
in 2007 compared to 150,000 cases of salmonelosis (Westrell
et al. 2009). In the United States, Campylobacter is the second most common cause of disease (gastroenteritis) responsible

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for approximately 845,000 illnesses annually and almost 100
deaths (CDC 2011). Campylobacter gastroenteritis is typically
associated with C. jejuni and Campylobacter coli.
Campylobacter is found in a range of animal hosts including cattle, lamb, pigs with poultry being implicated as a primary source (Niesen et al. 2006, Nachamkin 2007, Mor-Mur
and Yuste 2010). Additional sources of Campylobacter include
water, sewage, raw milk, raw meats, and vegetables (Meng and
Doyle 1998, Chan et al. 2001, Inglis et al. 2004, Nachamkin
2007). Prevalence levels of Campylobacter in food animals vary
significantly, while Campylobacter levels on pork products are
relatively low and may be related to postslaughter chill and drying effects, which significantly reduce the populations (Snijers
and Collins 2004). Raw and undercooked poultry appear to be
primary sources of Campylobacter associated with food-borne
illness (Olson et al. 2008, Mor-Mur and Yuste 2010, Newell
et al. 2010).
Campylobacter is a gram-negative organism and is a microaerobe with a requirement for low oxygen (microaerophilic) and a
temperature range of 35–42◦ C for growth. The organism is generally a poor competitor, is sensitive to low pH, temperatures less
than 30◦ C, pasteurization temperatures, and drying (Doyle and
Jones 1992). It does, however, appear to survive under refrigeration temperatures and freezing may cause cell reduction but
low levels of pathogen have been recovered (Blaser et al. 1980,
Jacobs-Reitsma 2000). The organism does not survive well in
foods and is easily destroyed by adequate cooking temperatures (Meng and Doyle 1998, Nachamkin 2007). Campylobacter is not capable of growth outside the host, but studies have
demonstrated the survival of this pathogen on kitchen surfaces

(Humphrey 2001).
The two major strains of Campylobacter implicated in the majority of human Campylobacter enteritis are C. jejuni and C. coli.
Typical cases of human campylobacteriosis include diarrhea, abdominal cramps, profuse diarrhea, nausea, and vomiting; other
symptoms include fever, headache, and chills, in some cases
bloody diarrhea can occur, recurrence of symptoms (relapse) is
often reported. Symptoms of illness are usually observed within
2-5 days of ingestion of contaminated food and can persist for
up to 2 weeks. The infectious dose required to cause illness is
relatively low and is estimated at approximately 500 organisms
(Robinson 1981, Black et al. 1988). Additional complications
recognized include reactive arthritis, pancreatitis, meningitis,
endocarditis, and Guillain–Barr´e syndrome a postinfection complication of campylobacteriosis that causes peripheral nervous
system paralysis resulting in a flaccid paralysis of the limbs,
which can be life threatening (Blaser and Engberg 2008, Jacobs
et al. 2008).
Outbreaks of campylobacteriosis typically occur in the summer months with most being sporadic in nature (Olson et al.
2008). Most outbreaks have been linked with improperly prepared or consumption of cross-contaminated, poorly handled
poultry (Alketruse et al. 1997, Friedman et al. 2000).
Of significant importance is the prevalence of antibiotic resistance to agents such as fluoroquinolones and macrolides,
two of the primary agents used to treat human disease (Engberg et al. 2001, Lutgen et al. 2009). Studies have reported