Int. J. Adv. Res. Biol. Sci. (2019).

6(10): 64-78

International Journal of Advanced Research in Biological Sciences

ISSN: 2348-8069
www.ijarbs.com
DOI: 10.22192/ijarbs Coden: IJARQG(USA) Volume 6, Issue 10 -2019
Review Article

DOI: http://dx.doi.org/10.22192/ijarbs.2019.06.10.007

A Review on Listeria monocytogenes in Food of Animal Origin

Enkeshe Loha Yada1* and Zenebech Katimar Anato2

1
Wolaita Zone Livestock and Fisheries office, SNNPR, Soddo, Ethiopia.
2
Wolaita Soddo Town Agricultural office, SNNPR, Soddo, Ethiopia.
Corresponding author: Enkeshe Loha Yada, Wolaita Zone Livestock and Fisheries office, SNNPR,
Soddo, Ethiopia, E-mail: [email protected]

Abstract
Listeria monocytogenes is the most important specie in the genus Listeria causing human and animal health threat. Among the
species only L. monocytogenes and L. ivanovii are considered pathogens L. monocytogenes is ubiquitous in the environment and
can be found in soil, water, faeces,silage, effluents foods and sewage. Even though freezing can lead to a reduction in L.
monocytogenes numbers, it can grow at temperatures as low as 0°Cin food during refrigerated storage. Human listeriosis is
usually associated with older adults, pregnant women, newborns and adults individuals with inadequate immune system.
Ingestion is the main transmission methods then it enters the intestine and binds to the receptors on the host cells to instigate
adhesion and internalization. The incidence of human listeriosis is low; the mortality rate is from 20% to 30%and with the highest
hospitalization rate. In general, L. monocytogenes can contaminate all types of animal origin food moreover contamination may
also occur after cooking by cross-contamination environmentally or via workers, surfaces and equipment’s. There have been
recent outbreaks of food poisoning associated with L. monocytogenesin different country. One-broth Listeria method, PCR (RTi--
-PCR), antibodybased tests, ELISA, immune-capture methods, molecular methods targeting different genes and biosensor
methods are different test methods used for analysis of L. monocytogenes. Highest resistance was detected against antibiotics so
recommended that effective cleaning and sanitation programs and safe handling procedures are important for ensuring a safe,
high quality food for consumer.

Keywords: Listeria, Food, Animal, Contamination, Characteristics.

Introduction monocytogenes [2]. The disease primarily affects older

adults, pregnant women, newborns and adults with
Listeria monocytogenes is the most important specie in weakened immune systems. Today, listeriosis is
the genus Listeria causing human health threat and regarded as a food-borne disease of serious public
spread worldwide with specific host range [1]. Even health concern. The incidence of human listeriosis is
though L. monocytogenes is mostly responsible of low (0.1–11.3 cases per million inhabitants), but it is
human listeriosis but occasionally infection with other increasing in Europe [3]. The mortality rate is reported
species such as L. seeligeri and L. ivanovii has been to be 20–30% [4]. In sum, the available literature
reported. Starting in the 1960s, as a result of the shows that L. monocytogenes has been reported from a
introduction and widespread use of refrigerators, wide variety of food types and responsible for
processed foods and extended shelf life foods became outbreaks and clinical manifestations in various
more associated with listeriosis due to L. countries of the world [4]. Most cases of listeriosis are
64
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

sporadic. Despite this, foodborne outbreaks due to Therefore, the objective of this paper is to review
L. monocytogenes have been associated with cheese, Listeria Monocytogens associated with food of animal
raw (Unpasteurized) milk, deli meats, salad, fish and origin and its diagnosis, analysis, control and
smoked fish, ice cream and hotdogs [4] also includes prevention.
poultry and ticks [4].
General characteristics of Listeria
Listeria commonly present in the dairy environment, monocytogenes.
on the farm and in the processing plant. On the farm,
animals have some pathogens itself, but Listeria is Description of the Organism
frequently present in manure and fermented silage. It
is most abundantly present in the humid areas, stable Listeria monocytogenes is a Gram-positive, non- acid
water including drains, coolers, washing areas and fast, non-spore forming, rod-shaped, facultative
floors [5]. The strong relation between occurrence of anaerobic an intracellular bacterium. It belongs to the
L. monocytogenes in raw milk and the infection of the genus Listeria along with six (6) species:L.
disease frequency was observed. Hence, a decrease in monocytogenes, L. innocua, L. seeligeri, L.
the number of cases per year in all populations was welshimeric, L. ivanovii and L. grayi. Of which L.
observed when unpasteurized milk was tested [6]. ivanovi and L.monocytogenes are pathogenic for mice
With increasing the consumption of manufactured and other animals [16]. Only two are considered
ready-to-eat foods in the whole world, it has become pathogens: L. monocytogenes which infects humans
known as an important opportunistic human foodborne and animals, and L.ivanovii which infects ruminants
pathogen [7]. (Although there have been rare reports of L. ivanovii
being isolated from infected humans) [17,18]. There
Despite an increasing rate of Listeriosis reported in are thirteen known serotypes of L. monocytogenes:
several European countries in recent years and other 1/2a, 1/2b, 1/2c, 3a, 3b, 3c, 4a, 4ab, 4b, 4c, 4d, 4e and
outbreaks in the United States [8] Canada [9,10] and 7. The serotypes most often associated with human
China [11] the occurrence and prevalence of the illness are 1/2a, 1/2b and 4b [19]. There are no strains
organism in food borne disease in Africa for examples, of L. monocytogenes with unique properties that lead
Nigeria is hardly reported [12]. But In Ethiopia, there to persistence and there are no mechanisms that can
is limited data regarding the prevalence of protect the organism when present in acidic juices,
L. monocytogenes in animal origin foods [13]. yogurt and salad dressing and modified CO2
atmosphere [20].
Lsteria monocytogenes is an important food bore
pathogen that cause septicemia, meningitis and Morphology, Growth and Survival Characteristics
gastroenteritis particularly in children, the elderly and They are facultative anaerobe that grows best under
immune suppressed individuals. It causes miscarriage reduced oxygen and increased carbon dioxide
in pregnant women. In addition to being a public concentration. Growth occurs at 4 to 45°C with an
health risk, L. monocytogenes is an economic burden optimum temperature of 30 to 37°C. Simple,
on the ready-to-eat (RTE) food industry. Ready-to-eat laboratory media support growth preferably at an
foods are the most vulnerable to L. monocytogenes as alkaline or neutral PH. Listeria tolerates 0.04%
they do not have a heating or other antibacterial step potassium tellurite 0.025% thallium acetate, 3.75%
between production and consumption. The economic potassium thiocyanate, 10% NaCl and 40% bile in
burden includes the cost of analysis of samples, the media. Most strains grow over a pH range of 5.5 to 9.6
costs, both financial and reputational, of recall of a [21]. Listeria monocytogenes has become known as an
contaminated product and the possible litigation costs, important opportunistic human food borne pathogen
if the food is shown to have caused disease [14]. The [7]. Freezing can also lead to a reduction in L.
standard microbiological methods for identification of monocytogenes numbers [22]. As L. monocytogenes
Listeria species are laborious and time consuming, can grow at temperatures as low as 0°C, it has the
requiring a minimum of five (5) days to recognize potential to grow, albeit slowly, in food during
listeria species and about 10 days to identify L. refrigerated storage. L. monocytogenes will grow in a
monocytogenes by confirmation test [15]. broad pH range of 4.0–9.6 [22]. It becomes more
sensitive to acidic conditions at higher temperatures
[2]. Like most bacterial species, L. monocytogenes
grows optimally at a water activity (aw) of 0.97.
65
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

However, L. monocytogenes also has the ability to In Ethiopia, Addis Ababa some studies show that there
grow at an awof 0.90 [22]. Survival in the presence of is the distribution of L. monocytogenes in foods of
salt is influenced by the storage temperature. Studies animal origin [13, 33]. L. monocytogenes can also be
have indicated that in concentrated salt solutions, the isolated from the surface and underground waters,
survival rate of L. monocytogenes is higher when the improperly fermented silage, sewage sludge, slaughter
temperature is lower [22]. It has greater heat tolerance wastes, animal and human faeces, foodstuffs, and food
than other non-spore forming bacteria; however, short- industry plants [34]. The occurrence of
time high temperature pasteurization is effective for L.monocytogenes in surface waters seems to be
killing listeria [21]. L. monocytogenes can grow under related to direct upstream land use, specifically, crop
both aerobic and anaerobic conditions; although it land and proximity to a dairy farms [34]. Silage is the
grows better in an anaerobic environment [22]. most common feed to harbor L. monocytogenes.
Listeria monocytogenes can consume limited numbers Chemical quality of silage, i.e. its PH and aerobic
of carbon sources for the energy with glucose. Thus, deterioration, affects the presence of L.
this microbe is essentially able to utilize different monocytogenes and the pathogen iscommonly found
sources of energy for the survival or growth in on poor quality silage [34].
gastrointestinal phase e.g. degradation of proteins,
polymers of carbohydrates, lipids and nucleic acids Listeria is most abundantly present in the humid areas,
[23]. stable water including drains, coolers, washing areas
and floors [5]. Epidemiological patterns of human
Epidemiology listeriosis include a background level of sporadic cases
with occasional outbreaks [35, 36]. A minimal
Persistence of Listeria monocytogene infective dose has not been determined in human
infection studies and estimates vary from 102 colony-
L. monocytogenes is ubiquitous in the environment forming units (cfu) to 109cfu, depending on the
and can be found in soil, water, faeces,silage, effluents immunological status of the host [37].
foods and sewage [24]. It has the ability to form
biofilms which can contribute to its ability to colonize Host factors that influence Listeriosis in Humans
food processing facilities. It is also resistant to many
of the stresses imposed in food processing such as salt Saha et al. [38] suggested that the first report was in
(Up to 10% salt), temperature (Refrigeration 1929 about human listeriosis, and in 1936 first
temperatures) and detergents (Many detergents). perinatal case was reported. Human llness is caused by
Therefore, it can survive in food processing eating the contaminated food which causes the
environments and become persistent. Such persistence infection [39] which may lead to serious and
of L. monocytogenes has been shown, often for many potentially life-threatening listeriosis. The presence of
years, at larger scale and smaller artisan facilities of listeriosis is usually associated with young, old,
different production sectors [25-27] Because pregnant and immunocompromised individuals with
L.monocytogenes is ubiquitous in the environment and inadequate immune system [40] typically presents as
frequently present in the processing environment, it septicemia, meningitis, or meningoencephalitis,
can contaminate foods includes fish, mammal, intrauterine infection; and sometimes death are
crustacean, poultry,and ticks [1] meat, soft cheeses reported [40]. Less frequently reported, but also at a
and ready to eat products are frequently [28] in cooked greater risk, are patients with diabetes, asthma,
foods due to post-processing contamination [14] the cirrhosis (Liver disease) and ulcerative colitis
food processing environment [29-31] in smoked fish (Inflammatory bowel disease) [19].
products and processing facilities [26] and ready-to-
eat food producing facilities [32]. Different rates of Virulence and infectivity
Listeria species prevalence were observed among the
various geographical areas under investigation that When L. monocytogenes is ingested, it may survive
there was a difference in contamination index of the stomach environment and enter the intestine where
animal origin by a range of pathogens between two it penetrates the intestinal epithelial cells.Furthermore,
different geographical locations in which different risk acidic conditions in the gastrointestinal tract and in
factors for each study region [28]. macrophages following phagocytosis can be
encountered by the pathogen and acid tolerance thus
enhances the virulence [41]. The organism is then
taken up by macrophages and non-phagocytic cells.
66
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

The L. monocytogenes surface protein internal in is women [45]. The incidence of human listeriosis is low
required for this uptake by non-phagocytic cells, as it (0.1–11.3 cases per million inhabitants), although rare,
binds to the receptors on the host cells to instigate the mortality rate of listeriosis is from 20 to 30 [46]
adhesion and internalization. The bacterium is initially 25% worldwide [47] but in those with underlying
located in a vacuole after uptake by a macrophage or disease or receiving immunosuppressant patients
non-phagocytic cell. L. monocytogenes secrete without adequate treatment up to 70% [48] and with
listeriolysin O protein, which breaks down the vacuole the highest hospitalization rate amongst known food
wall and enables the bacteria to escape into the borne pathogens > 95% [49] 91% [47]. Listeriosis
cytoplasm. Any bacteria remaining in the vacuole are affects domestic and wild animals, most often sheep
destroyed by the host cell. Once located in the and cattle, rarely goats, horses and poultry. Cows can
cytoplasm of the host cell, L. monocytogeneis able to excrete Listeria after miscarriage or during udder
replicate. L. monocytogenes is transported around the infections followed by mastitis, through milk. This
body by the blood, with most L. monocytogenes being was observed in some cases for several years.
inactivated when it reaches the spleen or liver. L. Contamination of milk by these bacteria can also be of
monocytogeneis able to utilize the actin molecules of faecal origin. Paralysis and circling movement was
the host to propel the bacteria into neighboring host observed in sheep affected by listeriosis in late stage
cells. In the case of invasive listeriosis, this ability to of the disease [50]. In animals, listeriosis usually
spread between host cells enables L. monocytogenes to occurs in five distinct clinical presentations, of which
cross the blood-brain and placental barriers [42, 43]. encephalitis is by far the most common form, followed
by abortions, whilst neonatal septicemia, mastitis and
Reservoir and Mode of Transmission kerato conjunctivitis/uveitis occur quite rarely. These
syndromes seldom overlap within the same animal or
Contamination may also occur via tools or hands, the same flock. Some authors speculate that
footwear and gloves and aprons of the personnel encephalitis occurs as a distinct syndrome and more
involved in manufacturing [34]. All food contact frequently than other clinical syndromes in farm
surfaces can be a source of contamination, but concern ruminants because immunity acquired through
especially rests on complex machinery that is hard to ingestion of contaminated silage protects against
clean and equipment that has contact with large septicemia and abortion but is not fully effective in
production like dairy processing plant [34]. Because of protection against encephalitis [51]. Furthermore,
the ubiquitous nature of L. monocytogenes, it is ruminants may commonly be asymptomatic intestinal
unrealistic to eliminate the organism from the food carriers of the organism [52].
chain and possible contamination sites will exist
throughout the chain [34]. Calves which develop Occurrences of Listeria monocytogenes in Different
septicemic are disease may acquire infection from Food of Animal Origin
contamination on the cow with subclinical bacteremia,
through the navel from the environment and also as a In general, pathogenic microorganisms can
congenital infection [21]. The encephalitic form of the contaminate raw milk in two ways. The first way is an
disease results from infection of the terminals of the endogenous contamination where the milk is
trigeminal nerve consequent to abrasion of the buccal contaminated by a direct transfer from the blood
mucosa from feed or browse or from infection of tooth (Systemic infection) to the milk or via an infection in
cavities. Spinal myelitis is believed to result from the udder called mastitis. The second way is an
growth to spinal nerves subsequent to body area exogenous contamination, where the milk is
infections [44]. contaminated during or after milking by the faeces, the
exterior of the udder and teats, the skin, the
Clinical Presentation and Course of the Disease in environment, etc [53]. Based on documents [54-57]
Human and Animals Listeria monocytogenes is considered as the main
microbiological hazards associated with raw milk
The average incubation period is 3 weeks that is from consumption among different pathogens. The EU
3 days to 3 months [19]. After ingestion of the summary report mentioned that non-compliance of L.
contaminated food, the bacteria that survive the acidity monocytogenes primarily occurred in soft and semi-
of the stomach enter the small intestine, cross the soft cheeses made from raw or low heat-treated cows'
epithelial barrier and then spread to the liver, spleen, milk [58].
central nervous system and the fetus in pregnant

67
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

Some factors which are involved in contamination monocytogenes is commonly found in comminuted
index between the region where the impermanent meats and is detected less often in tissues of freshly
cattle confinement, poor hygienic milking conditions, slaughtered pigs than in ground pork [62].
no cleaning, low milk production, and milk storage Contamination may also occur via tools or hands,
regions [59] have introduce a procedure for the quick footwear and gloves and aprons of the personnel
detection of Listeria monocytogenes in raw milk and involved in manufacturing [34]. Contamination of
soft cheese via merging of redox potential RTE poultry products can occur after cooking by
measurement methods for real time PCR and cross-contamination environmentally or via workers,
enrichment in which identification in an easy, time and surfaces and equipments [63]. While processed meat
the cost effective manner. Concerning butter, cream and poultry products are cooked to destroy Listeria,
and butter milk, there is less information available in these bacteria can recontaminate the product while it is
the scientific literature. But it is the main being handled, packaged or distributed [64].
microbiological hazards in butter made from raw milk
and it has been detected in butter. However, the risk of A more recent study reported 196 L. monocytogenes
infection after consumption of raw milk butter is isolates and demonstrated 3 genotypes out of total of
estimated to be relatively lower in comparison with 144 liquid whole egg samples [65]. studies were done
certain cheeses. L. monocytogenes also the main by [66] found 72.4% of fish and 44.4% of shellfish
microbiological hazards in and it has been detected in tested were found to be positive for Listeria species
cream. Even though pasteurization of raw milk [67, 68] reported 37.8% of sea food samples collected
destroys L. monocytogenes, this process does not from Mysore was positive for Listeria species. Listeria
eliminate later risk of contamination of dairy products species in tropical sea food of Keralaand India found
[60]. that L. innocua was the most prevalent species of
Listeria with an incidence rate of 28.7% and L.
The detection of Listeria monocytogenes in food is of monocytogenes with low prevalence i.e., 1.2% of the
particular concern in terms of consumer safety as this total samples tested [69]. Observed the higher
organism is capable of growing on both raw and incidence of L. monocytogenes (23.9%) in fish and
cooked meat at refrigeration temperature [61]. L. fish swab samples from Kerala [70].

Table 1. Different study in Africa on the Occurrences of L. monocytogenes from food of animal origin.

N Authors Country Number Diagnostic Overall Prevalence of L.monocytogenes by food

o and year of techniques prevalence category by food category
samples
1 [12] Nigeria 255 Plating on 63.5% Beef (88%), Chicken (64.7%) and fish (37.7%)
compact DRY
LS
2 [71] Ethiopia 384 ISO 11290-1 6.25% Raw meat (6.66%), Minced beef (12%), Fish
(6%), Pasteurized milk (0%), Raw milk (4%),
Cottage cheese (0%)
3 [72] Egypt 80 plating on 11.25% Retail local and imported pork by-products
PALCAM (11.25%)
4 [73] Ethiopia 240 ISDFM 4.1% Raw meat (6.8%), Raw milk (3.4%), Cottage
cheese (1.7%),
5 [74] Morocco 288 ISO 11290-1 5.90% Raw milk (8.33%),
6 [75] Algeria 227 AFNOR 2.6% Heat treated dairy products (3%), meat product s
V08055 (2.6%)
7 [76] Ethiopia 391 USFDA 5.4% Raw milk (13%), liquid whole egg (4.3%), raw
method beef (2.6%), cottage cheese (1%)
8 [77] Egypt 576 Oxoid and 14% Meat products (16%), poultry products (9%), sea
plated on food products (8%), dairy products (14%)
OXFORD aga
9 [78] Uganda 100 FDA-BAM 6.1% Rawmilk (13%), yoghurt (3%), fermented dairy
products (0%)
68
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

10 [79] Ethiopia 711 ISO 11290-1 4.8% Soft cheese (3.9%), meat products (3.7% to
5.1%)
11 [80] Nigeria 115 ISO 11290-1 25% Smoked fish (25%)
12 [81] South Africa 99 plating on 9.2% Fresh chicken (17%), frozen chicken (24%)
Oxford agar

Listeria monocytogenes Status in Ethiopia Outbreak of Listeria monocytogenes

Although foods of animal origin such as milk, cheese, The first confirmed role of food in the transmission of
meat and poultry are consumed well in Ethiopia, listeria infection was provided by the outbreak that
published information on the status of food borne occurred in 1977 in Boston (USA) in which 20
listeriosis caused by L. monocytogenes is very limited persons were reported to have developed listeriosis by
and incomplete in both in the veterinary and public eating contaminated raw celery of tomatoes and
health sectors [5]. But some study for example: by lettuce [21]. There have been recent outbreaks of food
[82] showed that Listeria species exist in the Ethiopian poisoning associated with L. monocytogenes [13]. In
food production system and his study detected L. the year 1986, the WHO has recognized L.
monocytogenes and L. innocua were found. In monocytogenes as an important emerging food-borne
Ethiopia, a study has shown the presence and pathogen. There have been many recent high-profile
distribution in a variety of raw and ready- to-eat food outbreaks of listeriosis worldwide that have resulted in
products in Addis Ababa with a prevalence of 5.1% numerous fatalities [84] reviewed a particular issue of
[73, 83] described 4.1% of prevalence from raw meat listeriosis-associated brain stem encephalitis [84].The
and dairy products like raw milk, cheese and cream listeriosis presence in human population is low in the
cake collected from the capital and five neighboring percentages1%, but with high fatal outcome 30% [85].
towns in Ethiopia. According to [13] research study Low incidence of human listeriosis is low annually
the overall prevalence of Listeria species was 28.4% causes 2500 of serious cases of illness with
and specifically that of L. monocytogenes was 5.6%. approximately 500 deaths [86]. [87] suggested that
Taking the prevalence of Listeria species into 250 death rate, 1600 invasive infection and 1500
consideration, cheese was found to be highly hospitalizations per year by listeria species. Of those
contaminated at 60%, followed by pasteurized milk individuals with laboratory confirmed listeriosis, there
samples (40%), raw milk (18.9%) and yoghurt (5%). is a 94% hospitalization rate and 15.9% death rate.
Considering the prevalence of Listeria monocytogenes Hazard of listeriosis in pregnant women is ten times
only, raw milk had the lowest contamination while greater than the common people and four times higher
cheese had the highest, followed by pasteurized milk in individuals aged sixty-five years or older. Back
and yoghurt. The study shows as raw milk and milk ground information about outbreak of listeriosis can be
products produced in urban and per urban areas of found in ECDC, CDC and WHO disease fact sheets
central Ethiopia were contaminated with pathogenic [88-90]. During the period 2012–2016, between 1 754
bacteria, L. monocytogenes. Finally the study and 2 555 Listeria monocytogenes cases were reported
concluded that milk and milk product contamination annually to the European Surveillance System
with L. monocytogenes in the central highlands of (TESSy) by 30 EU/EEA countries [88]. Event
Ethiopia is an issue of public health significance. The background information in 2017, Finland reported in
presence of L. monocytogenes in raw bovine milk and EPIS-FWD an urgent inquiry describing a cluster of L.
especially milk products such as pasteurized milk monocytogenes PCR sero group IVb, MLST ST6
warrants an urgent regulatory mechanism to be put in confirmed by WGS (in-house cg MLST scheme), with
place. High public health concern as most of the milk 13 cases detected from different parts of Finland
and milk products in Ethiopia are consumed in raw between 2016 - 2017. As of 2017, nine EU/EEA
forms without being treated with sufficient heat. countries had replied to the urgent inquiry. Four
Considering the high fatality rate for listeriosis, countries reported cases that could be linked
especially in the risk groups, this rate of prevalence is microbiologically to the Finnish cluster based on the
of high public health concern [13]. WGS data using either cg MLST [91, 92] or SNP
analysis (In-house pipelines).

69
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

2.9. Methods for detection and Analysis of Listeria There is a wide range of different test methods for
monocytogenes Listeria spp. and L. monocytogenes that have been
reviewed by [97 these include antibody-based tests,
Methods of detection enzyme linked immunosorbent assay (ELISA),
immune-capture methods, molecular methods
L. monocytogenes contamination usually occurs in targeting different genes and biosensor methods.
very low numbers both in foods and in the processing
environment so it is vital that any analysis performed Characterizations of isolates
includes one or more enrichment steps which inhibit
other microflora, and allow both the increase of L. In order to identify the source or route of
monocytogenes in sufficient numbers to allow contamination, it is necessary to identify the strain
detection and the recovery of injured/stressed cells. type of L. monocytogenes contaminating the food or
The standard microbiological methods for the processing environment rather than just give a
identification of Listeria species are laborious and time positive/negative result. Differentiation of L.
consuming, requiring a minimum of five (5) days to monocytogenes strains by serotyping is one of the
recognize listeria spp and about 10 days to identify L. oldest methods of typing and is based on the somatic
monocytogenes by confirmation test [93]. It is (O) and flagellar (H) antigen differences between
therefore necessary to use a chromogenic medium that strains. As more exacting typing techniques have since
will give results within 24 hrs [12]. Three methods of been developed, serotyping of strains now offers little
analysis are most commonly used: the International in terms of strain identification but can be helpful in
Standard (ISO-11290) method which uses a two-step the characterization of strains [98]. However, to
enrichment in Fraser broth, the United States further differentiate strains into their serotype, testing
Department of Agriculture (USDA) method which with antisera needs to be performed, it can be
uses a two-step enrichment in University of Vermont prohibitively expensive. Some reactions in antisera
media (UVM) and the One-broth Listeria method testing can be variable, for instance, currently
which has been approved for use by the Association serotypes 4b and 4e cannot be separated by this
Française de Normalisation (AFNOR) and takes method. The vast majority of listeriosis outbreaks,
considerably less incubation time and yields results in approximately 90%, are caused by 1/2b and 4b
2 days as opposed to the 4-5 days needed for the other serotypes, both of which are commonly found in food
two methods [27]. All these methods involve plating and food processing facilities. In general, serotype
on Listeria selective agar (Traditional or chromogenic 1/2a has been isolated most frequently from food and
agars) and require confirmation of isolates as L. the food processing environment [99,100]. Although,
monocytogenes by biochemical or molecular tests. The it is thought that some serotypes may be generally
use of real-time PCR (RTi-PCR), in combination with more virulent than others, currently all L.
traditional culture, to detect the presence or absence of monocytogenes strains must be treated as virulent.
Listeria has also been explored in recent years [94, Therefore, the identification of certain serotypes in a
95]. food or a processing facility does not mean that they
will or will not cause disease. The gold standard for L.
By amplifying Listeria specific genes through PCR monocytogenes sub-typing remains pulsed field gel
and quantifying them by the detection of a fluorescent electrophoresis (PFGE), although other methods do
probe attached to the DNA fragments, even low offer advantages. PFGE is quite expensive, takes
numbers of the bacteria can be detected within a few several days and requires trained staff to perform.
hours (After enrichment) as opposed to the several However, it offers better discriminatory power than
days it takes to complete traditional plating most other methods and can be compared between
techniques. For best use, RTi-PCR should be labs if performed according to international
combined with the traditional methods so that isolates standard practices [101]. After characterizing the
can be obtained from the direct detection of L. molecular diversity of isolates in the environment in
monocytogenes in food as it lacks the required question, putative routes of transmission and/or
sensitivity, may be subject to inhibition by food sources of entry into the environment can be identified
ingredients and can detect the presence of DNA from [102] identified three potential contamination
live as well as dead cells [6, 96] and studied that the scenarios that can increase the risk of food
recent reports showed the immediate detection of contamination, hot-spot contamination (Where a
Listeria monocytogenes by PCR curve analysis. specific area is contaminated), widespread

70
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

contamination (Where contamination is spread For example, in the Quargel cheese outbreak in
throughout the facility) and sporadic contamination Austria in 2009/2010, WGS was used to identify 2
(where non-persistent contamination occurs on an distinct 1/2a L. monocytogenes strains (QOC1 and
irregular basis). Visualization of the contamination on QOC2) which overlapped to form the outbreak [110].
a facility map can help identify the putative Through whole genome sequencing (WGS), specific
contamination routes [103]. Thus, control strategies genes which contribute to invasion and survival were
can be adjusted/ targeted to remove the source of also identified including the presence of a vip
contamination and interrupt the route of transfer to the homologue in QOC2 which encodes a surface protein,
food. Analysis of such results can not only identify likely responsible for the higher invasion efficiency of
persistent strains, but can also identify an area which QOC2 in comparison with QOC1. As costs continue to
may be colonized by a particular strain, leading to fall, WGS is increasingly being used in outbreak
possible recontamination events. It can also be used to investigations as it offers a much more comprehensive
prevent the spread of strains throughout the facility. overview of a strain and gives a significantly higher
Multilocus sequence typing (MLST) is also commonly confidence in strain identification.
used in strain typing, by sequencing a specific set of
alleles of housekeeping genes and analyzing the Challenge to determine the ability of food to
variations in the sequences, which allows support growth of Listeria monocytogenes
identification of strain differences.
Certain foods are categorized in a higher risk category
Although less discriminatory than PFGE, the for contamination with L. monocytogenes. These are
evolutionary distance between strains can be ready-to-eat (RTE) foods since the heat step of
measured, by inspecting the number of alterations in cooking, which would kill any L. monocytogenes
the sequences, which cannot be performed by PFGE present, is missing in these foods. Thus, if the food
[104]. PCR to detect different genes present in L. product is able to support the growth of L.
monocytogenes strains is also commonly used for monocytogenes, bacterial numbers can reach high
strain characterization. The presence/absence of levels, even at refrigeration temperatures, posing a
different genes can be a good indication of whether or health risk for consumers. Determining the ability of
not a strain is virulent or whether it possesses genes RTE foods to support the growth of L. monocytogenes
which may help it to persist in a food processing is important, especially in those jurisdictions where
facility. Several genes, such as the stress survival islet there is no zero tolerance policy for L. monocytogenes
SSI-1 and the Tn6188transposon, which confers (e.g. Europe, Canada and Australia). The ability of L.
resistance to certain quaternary ammonium monocytogenes to grow in food products may be
compounds, have been identified which appear to estimated based on specifications of the physico-
confer advantages to strains which may help them to chemical characteristics of the product, consultation of
survive in the seemingly inhospitable environment of a the available scientific literature, or predictive
processing facility [105, 106]. mathematical modeling. Such predictive models are
useful, but for many reasons, including the possibility
Similarly, several genes which contribute to virulence of overestimation/underestimation of growth in food
have been identified, for example listeriolysin S (LLS) products, in most cases growth assessment will
and act A, and the use of PCR to detect these genes involve laboratory -based studies, so-called challenge
can help to evaluate strains ability to cause disease tests. From a public health perspective, overestimation
[107]. Other options for characterization of L. of growth is a fail-safe’ scenario, although such
monocytogenes isolates include Multiple-Locus overestimation can be inaccurate from a food
Variable Tandem Repeat Analysis (MLVA), producer‘s perspective. For example, in 40% of cases
ribotyping, phenotypic or biochemical arrays and Combase predicted growth in cheese when no growth
Fourier Transform infrared spectroscopy [108]. In was seen in growth experiments [111]. It was further
recent years, the price of whole genome sequencing shown that the growth characteristics of L.
(WGS) has lowered significantly allowing the use of monocytogenes were different in liquid and solid
WGS in more routine applications. As opposed to matrices [112].
PFGE or MLST, WGS examines the entire sequence
of a genome, rather than just part of it and so gives a
much higher strain differentiation [109]. Individual
genes can also be examined through the use of WGS.

71
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

Regulations Relating to L. monocytogenes more practical approach. Such control can be achieved
by attention to detail in hygiene strategies, monitoring
In Africa, in general, there is little awareness or occurrence of the organism or using novel control
regulation relating to L. Monocytogenes. For example, methods such as bacteriocins (Are ribosomally-
a recent amendment to the South African Foodstuffs synthesised peptides that are pore-forming agents,
[85] referring to microbiological standards has nothing which act by disrupting the integrity of the target
on Listeria spp. The Dairy Standard Agency (DSA) cell membrane) and bacteriophage (Are viruses that
has guidelines in its Codes of Practice relating to L. infect and can kill ) bacteria and are logical candidates
monocytogenes in raw milk for final consumption, for bio -control of L. monocytogenes in food [14].
pasteurised milk, UHT milk, cream and salted butter The potentially long incubation time for
[113]. In these products, the guidelines recommend the L.monocytogenes to cause disease can also make it
absence (in 25 g) of L. monocytogenes in raw milk for difficult to trace the disease to a specific food and
consumption and in other products. In general, source of contamination [3]. It is therefore important
companies that export, use the relevant regulation in to remove as many sources of contamination as
the country they export to. One South African possible from the food processing environment to
voluntary standard (South African National Standard reduce the possibility of food contamination [14].
[SANS] 885:2011) that specifically refers to the
prevalence of L. monocytogenes in processed meat Non-food contact surfaces, especially floors and
products, allows a maximum of 100 cfu/g at the end of drains, can be a reservoir of L. monocytogenes in the
shelf life. In Europe, Regulation (EC) No 2073/2005 meat industry [34]. Care has to be taken to clean and
sets the microbiological criteria for L. monocytogenes sanitize these sites, because they may contaminate
in foods that must be complied with. This regulation other sites in the food processing facility. Cooking is
primarily covers RTE food products and requires that effective methods to eliminate L. monocytogenes from
L. monocytogenes must be absent from foods (10 x 25 meat. The ideal processing method would improve the
g) intended for infants and for special medical shelf life and safety of the meat product, not
purposes , and allows different criteria depending on compromise organoleptic or nutritional value is
the ability of the food product to support growth of L. convenient and economical to apply, and not cause
monocytogenes. In Canada and Australia/New- objections by consumers [116]. People at risk of
ZealandCriteria-for-Listeria-monocytogenes-in-ready- infection such as pregnant woman or person with a
to-eatfoods.aspx, the regulations are in line with weak immune system should take additional
European regulations, allowing a differentiation precautions with these types of foods. It is pertinent to
between foods that can and cannot support growth. mention that proper hygiene, and sanitation in food
However, in the USA there is zero tolerance ‘of L. establishments, pasteurization of dairy products,
monocytogenes (Absence in 5 x 25 g of food is cooking of meat, and fish and health education of high
required at all times, and in the processing risk groups about the severity of disease, mode of
environment). transmission, and preventive measure will certainly
help to reduce the incidence of listeriosis [117].
Treatment of L. monocytogenes Infections in
Human and Animals Conclusion
Listeria species resistant to penicillin G and Listeria monocytogenes is the most important specie in
tetracycline, but some are less resistant to the genus Listeria causing human and animal health
chloramphenicol, amoxicillin acid, clindamycin, threat. Its epidemiological studies would help in better
kanamycin and erythromycin [114]. Highest resistance understanding of the sources of infection and their risk
detected against penicillin, nalidixic acid and assessment, routes of transmission, clinical forms and
erythromycin, with all 78 (100 %) tested for Listeria better management of the infection. Standard and
species presenting resistance [115]. hygienic operating methods in the farming, processing
and marketing of foods are the way forward to reduce
Prevention and Control the incidence of listeriosis. Listeria monocytogenes
and other Listeria species isolated from food of animal
As L. monocytogenes is a ubiquitous organism, its origin animal with significant percentage. The
complete elimination is an unrealistic aim. Control is a contamination sources of Ready-to-eat foods of animal
origin are more likely to be associated with
72
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

insufficient hygienic practices and improper handling. 10.Cartwright, E.J., K.A. Jackson, S.D. Johnson, I.
The presence of this organism in these undercooked Graves , B. Silk and B. Mahon, 2013. Listeriosis
food products could be a potential risk for consumers. outbreaks and associated food vehicles in United
From the above conclusion the following States 1998-2008.Emerging Infectious Diseases,
recommendations are forwarded: 19:1-9.
11.Wang, H.I., K.G. Ghanem, P. Wang, S. Yang and
 Effective cleaning and sanitation programs and safe T.S. Lis, 2013. Listeriosis at a tertiary care hospital
handling procedures are important in Beijing. High prevalence of non-clustered
 Training for carrying out standard sanitary, hygiene healthcare associated cases among adult patients.
and technical operations. Clinical Infection Diseases, 56:666-676.
 Further studies on the occurrence of Listeria species 12.Lennox, Josiah ,A., O. Etta, Patience, E. John,
in various food products should be carried out. Godwin , Henshaw and E. Effiom,2017.
Prevalence of Listeria monocytogenes in Fresh
References and Raw Fish, Chicken and Beef, 3(4): 1-7
13.Eyasu, T., Seyoum , Daniel A. Woldetsadiˡ, Tesfu
1. Peer, M., R. Nasir, D. Kakru, B. Fomda, M. Wani K. Mekonen, Haile A. Gezahegn and Wondwossen
and Q. Hakeem, 2010. Listeria monocytogenes A. Gebreyes, 2015. Prevalence of Listeria
meningoencephalitis in an immunocompetent, monocytogenes in raw bovine milk and milk
previously healthy 20month old female child. products from central highlands of Ethiopia,
Indian J Med. Microbiol., 28:169 171. 9(11):1204-1209.
2. Lamont, R., J. Sobel, S. Mazaki-Tovi, J. 14.Dara, L., A. Avelino, J. Piet and J. Kieran , 2015.
Kusanovic, E. Vaisbuch, S. Kim, N. Uldbjerg and Listeria monocytogenes in food: Control by
R. Romero, 2011. Listeriosis in human pregnancy: monitoring the food processing environment, 1996-
a systematic review. J Perinat Med, 39:227-236. 0808
3. Goulet, V., C. Hedberg, A. Le Monnier and H. De 15.Weinstein, K.B., 2016. Listeria monocytogenes
Valk, 2008. Increasing incidence ofListeriosisin infection (Listeriosis). Medscape, 13(2):46-52.
France and other European countries. Emerg Infect 16.Khanzadi, S. and A. Jamshidi, 2011. The presence
Dis, 14:734–740. of Listeria monocytogenes in raw milk samples
4. Swaminathan, B. and P. Gerner-Smidt, 2007.The in Mashhad, Iran. Iran J Vet Res, 11.
epidemiology of human listeriosis. Microbes Infect 17.Guillet, C ., O. Join-Lambert, A. Le Monnier, A.
(Institut Pasteur), 9:1236—43. Leclercq, F. Mechai, M. Mamzer-Bruneel, M.
5. Seyoum, T., Daniel A. Woldetsadik, Tesfu K. Bielecka, M. Scortti, O. Disson, P. Berche, J.
Mekonen, Haile A. Gezahegn, Wondwossen A. Vazquez-Boland, O. Lortholary and M. Lecuit,
Gebreyes, 2015. Prevalence of Listeria 2010. Human Listeriosis Caused by Listeria
monocytogenes in raw bovine milk and milk ivanovii. Emerg. Infect. Dis., 16:136-138.
products from central highlands of Ethiopia, 18.Konosonoka, I., A. Jemeljanovs, B. Osmane, D.
9(11):1204-1209. Ikauniece and G. Gulbe, 2012. Incidence of
6. Latorre, A., A. Pradhan, J. Van Kessel, J. S. Karns, Listeria spp. in dairy cows feed and raw milk in
K. J. Boor D. H. Rice and Y. H. Schukken, Latvia. ISRN Vet Sci,transform infrared
2011.Quantitative risk assessment of listeriosis due spectroscopy. J Food Prot, 78(3): 540-548.
to consumption of raw milk. J Food Prot, 74:1268- 19.Foodborne pathogenicmicroorganisms (FDA),
1281. 2012. Bad bug book: Foodborne
7. Ponniah, J., T. Robin, M. Paie, S. Radu, pathogenicmicroorganisms and natural toxins
F.Mohamad Ghazali and Y. Cheah , 2010. handbook, 2nd ed. US Food and Drug
Detection of Listeria monocytogenes in foods. Administration, Silver Spring, 100–104.
FOOD RES INT, 17:1-11. 20.Ryser, E.T. and E.H. Marth, 2007. CRC Press,
8. Allerberger, F. and M. Wagner, 2010. Listeriosis: a Taylor & Francis Group, Boca Raton, Florida,
resurgent food borne infection. Journal of Clinical USA, 85-110
Microbiology Infection, 16: 16-23 21.Tewodros, F. and F. Atsedewoyne,
9. Taillerfer, C., M. Boucher, C. Lafemeries and L. 2012.Listeriosis.in Small Ruminants: Advance In
Merin, 2010. Prenatal listeriosis, Canada’s 2008 Biological Research, 6(6): 202-209.
outbreaks. Journal of Obstertrics and Gynaecology,
32:45-48.
73
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

22.Lado, B. and A. Yousef, 2007. Characteristics of 32.Kovačević, J., L. McIntyre, S. Henderson and T.
Listeria monocytogenesimportant to food Kosatsky,2012.Occurrence and distribution of
processors. Ch 6 In: Ryser ET, Marth EH (eds) listeria species in facilities producing ready-to-eat
Listeria, listeriosis and food safety. 3rd ed, CRC foods in British Columbia, Canada. J. Food Prot,
Press Taylor & Francis Group, Boca Raton, 157– 75:216-24.
213 . 33. Cerva, C., C. Bremm, E.M. Dos Reis, A. Bezerra,
23.Tsai, H. and D.A. Hodgson, 2013. Development of M. Loiko, C. Da Cruz CEF, A. Cenci A and
a synthetic minimal medium for Listeria F.Q.Mayer, 2014. Food safety in raw milk
monocytogenes. Appl Environ Microbiol, 69: production: risk factors associatedto bacterial DNA
6943–5. contamination. Trop Anim Health Prod.DOI
24.Singh, J., V.K. Batish and S. Grover, 2012. 10.1007/s11250-014-0580-y.
Simultaneous detection of Listeria 34.Tereza, G. and K. Renata, 2012.Outdoor
monocytogenes and Salmonella spp. in dairy environment as a source of Listeria
products using real time PCR-melt curve analysis. monocytogenes in food chain.Czech Journal of
Int J Food Sci Tech, 49:234-239. Food Science, 30, 83.
25.Fox, E., K. Hunt, M. O'Brien and K. Jordan, 2011. 35.Gillespie, I., P. Mook, C. Little, K. Grant and G.
Listeria monocytogenes in Irish Farmhouse Adak, 2010. Listeria monocytogenes infection in
cheese processing environments. Int. J. Food the over-60s in England between 2005 and 2008: A
Microbiol.145, Supplement, 1:S39-S45. retrospective case-control study utilizing market
26.Tocmo, R., K. Krizman, W.J. Khoo, L.K. Phua, research panel data. Foodborne Pathog Dis, 7:
M. Kim and H-G. Yuk, 2014. Listeria 1373-1379.
monocytogenes in Vacuum-Packed Smoked Fish 36.Нom, D., N. Strachan, K.Goodburn, O. Rotariu and
Products: Occurrence, Routes of Contamination, M. Hutchison, 2012. A review of the published
and Potential Intervention Measures. Comp. Rev. literature and current production and processing
Food Sci. Food Safety, 13:1735-1739 practices in smoked fishprocessing plants with
27.Gomez, D., L. Pilar Iguacel, M. Rota, J. emphasis on contamination by Listeria
Carraminana, A. Arino and J. Yanguela, 2015. monocytogenes. Final FSA report.
Occurrence of Listeria monocytogenes in Ready- 37.Jemmi, T. and R. Stephan, 2006. Listeria
to-Eat Meat Products and Meat Processing Plants monocytogenes: foodborne pathogen and hygiene
in Spain, Foods, 4:271-282. indicator. Rev Sci Tech 2Int Epiz, 25: 571-580.
28.Cerva, C., C. Bremm, E. dos Reis, A.Bezerra, M. 38.Saha, M., C. Debnath and A. Pramanik, 2015.
Loiko, C. da Cruz , A. Cenci and F. Mayer, 2014. Listeria monocytogenes: An Emerging Food Borne
Food safety in raw milk production: risk factors Pathogen. Int. J. Curr. Microbiol. App. Sci, 4(11):
associatedto bacterial DNA contamination. Trop 52-72.
Anim Health Prod.DOI 10.1007/s11250-014-0580- 39.Atil, E., H. Ertas and G. Ozbey, 2011. Isolation and
y. molecular characterization of Listeria species .
29.Vongkamjan, K., S. Roof, M.J. Stasiewicz and M. from animals, food and environmental samples.
Wiedmann, 2013. Persistent Listeria Vet Med, 56:386-394
monocytogenes subtypes isolated from a smoked 40.Alemayehu, H., S. Gebretsadik , K. Huruy, T.
fish processing facility included both phage Kassa and N. Kebede, 2011. Isolation and
susceptible and resistant isolates. Food Microbiol, characterization of Listeria monocytogenes and
35:38-48. other Listeria species in foods of animal origin in
30.Jami, M., M. Ghanbari, M. Zunabovic, K. Domig Addis Ababa, Ethiopia. J Infect Public Health, 4:
and W. Kneifel, 2014. Listeria monocytogenes in 22-29.21.
Aquatic Food Products-A Review. Comp. Rev 41.Changyong, C., C. Jianshun, S. Ying, F. Chun,
Food Sci. Food Safety, 13:798-813. L.Yuan, X. Ye, S. Houhui and F. Weihuan, 2013.
31.Nakari , U.M., L. Rantala, A. Pihlajasaari, S. Listeria monocytogenes ArcA contributes to acid
Toikkanen, T. Johansson, C. Hellsten, S.M. Raulo, tolerance. Journal of medical microbiology, 62:
M. Kuusi, A. Siitonen and R. Rimhanen-Finne, 813-821.
2014. Investigation of increased listeriosis revealed 42.Kuhn, M. and W. Goebel, 2007. Molecular
two fishery production plants with persistent virulence determinants of Listeria monocytogenes.
Listeria contamination in Finland in 2010. Ch 5 In: Ryser ET, Marth EH (eds) Listeria,
Epidemiol. Infect, 142:2261-2269
74
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

listeriosis and food safety. 3rd ed, CRC Press these risks and benefits.Available online
Taylor & Francis Group, Boca Raton, p. 111–155 http://www.favv afsca.fgov.be/wetenschappelijk
43.Bonazzi, M., M. Lecuit and P. Cossart, 2009. comite/adviezen/_documents/ADVIES15-2011_
Listeria monocytogenesinternalin and E-cadherin: NL_DOSSIER2010-25.pdf. Last accessed,
From structure to pathogenesis. Cellular 13.10.14
Microbiology, 11(5):693–702 55.Claeys, W. L., S. Cardoen, G. Daube, J. De
44.Ikeh, M., S. Obi, D. Ezeasor, I. Ezeonu and A. Block, K. Dewettinck and K. Dierick, 2013. Raw
Moneke, 2010 . Incidence and pathogenicity profile or heated cow milk consumption: review of risks
of Listeriasp. Isolated from food and environmental and benefits. Food Control, 31,251e262. Dairy
samples in Nsukka, Nigeria.Afr J Biotechnol, Standards Agency
9:4776—82. 56.Verraes, C., W. Claeys, S. Cardoen, G. Daube, L.
45.Ramaswamy, V., V. Cresence, J. Rejitha, M. De Zutter and H. Imberechts, 2014.A review of the
Lekshmi, K. Dharsana, S. Prasad and H. Vijila, microbiological hazards of raw milk from animal
2007. Listeria--review of epidemiology and species other than cows.International Dairy
pathogenesis. J Microbiol Immunol Infect. Feb, Journal, 39: 121e130.
40(1):4-13. 57.EFSA ,2015. Scientific opinion on the public
46.Sergelidis, D. and A. Abrahim, 2009. Adaptive health risks related to the con-sumption of raw
response of Listeria monocytogenesto heat and its drinking milk.EFSA Journal, 13: 3940.
impact in food safety.Food Control, 20:1-10. 58.EFSA and ECDC, 2015. The European summary
47.DeNoordhout, C., B. Develeesschauwer, F. report on trends and sources of zoonoses, zoonotic
Angulo, G. Verbeke, J. Haagsma, M. Kirk, agents and food-borne outbreaks in, 2013.
A.Havelaar and N. Speybroeck, 2014. The global 59.Erdősi, O., K. Szakmár, O. Reichart, Z. Szili, N.
burden of listeriosis: a systematic review and meta- László, P. Székely Körmöczy and P. Laczay, 2014.
analysis. The Lancet Infectious Diseases, Rapid detection of Listeria monocytogenes in
14(11):1073-1082. raw milk and soft cheese by a redox potential
48.World Health Organization (WHO), 2008. measurement based method combined with real-
Foodborne disease outbreaks: Guidelines for time PCR. ACTA VET HUNG, 62(3): 304-316.
investigation and control. Section, 6.3. 2008. 60.Centre for Disease Control and Prevention (CDC),
49.Scallan, E., 2011. Foodborne illness acquired in the 2013. When Food Bites Back. Protecting people
United States--major pathogens. Emerg. Infect. from deadly Listeria food poisoning. Available at:
Dis., 17:7-15. 61.Walker, S.J., P. Archer and J.G. Bank, 2009.
50.Kasalica, A., V. Vukovic, A. Vranjes and N. Growth of Listeria monocytogenesat refrigeration
Memisi, 2011. Listeria monocytogenes in milk temperature. Journal of Applied Bacteriology,
and dairy products. Biotech Anim Husbandry, 68:157-162.
27:1067-1082. 62.Miyasaki, K. N., E. C. Chiarini, A. de Souza
51.Muhammed, W., D. Muleta, Y. Deneke, A. Santana, M. T. Destro, M. Landgraf and B. D. G.
Gashaw and M. Bitew , 2013. Studies on de Melo Franco, 2009. High prevalence, low
occurrence of Listeria monocytogenes and other counts and uncommon serotypes of Listeria
species in milk and milk products in retail market monocytogenes in linguiça, a Brazilian fresh pork
of Jimma town, Ethiopia. Asian J Dairy Food Res, sausage. Journal of meat science, 83: 523-527.
32: 35-39. 63.Osaili, T.M., A.R. Alaboudi and E.A. Nesiar, 2011
52.Oevermann, A., Z. Andreas and M. Vandevelde, . Prevalence of Listeria spp. and antibiotic
2010. Rhombencephalitis caused by Listeria susceptibility of Listeria monocytogenes isolated
monocytogenes in humans and ruminants: A from raw chicken and ready-to-eat chicken
zoonosis on the rise? Interdiscip Perspect Infect products in Jordan. Food Control, 22: 586-590.
Dis, 632513. 64.Lekroengsin, S., S. Keeratipibul and K.
53.Jamshidi, A. and S. Khanzadi, 2011. The presence Trakoonlerswilai, 2007. Contamination profile of
of Listeria monocytogenes in raw milk samples Listeria spp. in three types of ready-to-eat chicken
in Mashhad, Iran. Iran J Vet Res.,11.. meat products. J Food Prot, 70: 85-89.
54.Sci Com, 2011.Advice 15-2011 of 14 October 65.Rivoal, K., S. Quéguiner, E. Boscher, S. Bougeard,
2011 of the Scientific Committee of the FASFC on G. Ermel and G. Sal-vat, 2010. Detection ofListeria
the riskebenefit evaluation of raw cow milk monocytogenesin raw and pasteurized liquid whole
consumption and the effect of heat treatment on
75
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

eggs and characterization by PFGE. Int J Food in foods of animal origin in Addis Ababa, Ethiopia,
Microbiol,138:56-62. 4: 22—29.
66.Anonymous, 2011. Listeria Regulation. Food 77.El-Shenawy, M., M. El-Shenawy, J. Manes and J.
Control, 22(9):1477-1549. Soriano, 2011. Listeriaspp.in street-vended ready-
67.Vinoth Kumar, R., K. Arunagiri and T. Sivakumar, to-eat foods. Interdisciplinary perspectives on
2013 . Studies on pathogenic Listeria infectious diseases, 2011.
monocytogenes from marine food resources. doi:10.1155/2011/968031.
International J Curr Microbiol App Sci, 1(1): 86- 78.Mugampoza, D., C. Muyanja , P. Ogwok, M.
93. Serunjogi and G. Nasinyama, 2011. Occurrence of
68.Moharem, A.S., A.P. Charith Raj and G.R. Listeria monocytogenes in bulked raw milk and
Janardhana, 2007. Incidence of Listeria species in traditionally fermented dairy products in Uganda.
sea food products of Mysore, India. J Food Safety, African J. Food, Ag, Nut. Dev., 11:4610-4622.
27: 362-372. 79.Mengesha, D., B. Zewde, M. Toquin, J. Kleer, G.
69.Das, S., K. Lalitha, N. Thampuran and P. Hildebrandt and W. Gebreyes, 2009. Occurrence
Surendran, 2012. Isolation and characterization of and distribution of Listeria monocytogenes and
Listeria monocytogenes from tropical sea food other Listeria species in ready-to-eat and raw meat
of Kerala, India. Ann Microbiol, products. Berl Munch Tierarztl Wochenschr, 122:
DOI10.1007/s13213-012-0566-9. 20-24.
70.Swetha, C.S., T. Madhava Rao, N. Krishnaiah and 80.Salihu, M., A. Junaidu, S.B. Manga, M.L.
A.Vijayakumar, 2012.Detection of Listeria Gulumbe, A.A. Magaji, A. Ahmed, A.Y. Adamu,
monocytogenes in fish samples by PCR assay. A. Shittu and I. Balarabe, 2008. Occurrence of
Ann Biol Res., 3(4): 1880-1884. Listeria monocytogenes in smoked fish in
71.Garedew, L., A. Taddese, T. Biru, S. Nigatu, E. Sokoto, Nigeria. Afr. J. Biotechnol, 7:3082-3084.
Kebede, M. Ejo, A. Fikru and T. Birhanu, 2015. 81.Van Nierop, W., AG. Duse, E. Marais, N. Aithma,
Prevalence and antimicrobial susceptibility profile N. Thothobolo, M. Kassel, R. Stewart, A.
of Listeria species from ready-toeat foods of Potgieter, B. Fernandes, JS. Galpin and SF.
animal origin in Gondar Town, Ethiopia. BMC Bloomfield, 2005. Int J Food Microbiol. 99(1): 1-6
Microbiol, 15:100. doi:10.1186/s12866-015-0434- 82.Firehiwot Abera Derra, Susanne Karlsmose,
4. Dharam P. Monga Abebe Mache, Christina Aaby
72.Hakim, A., A. Abuelnaga , A. Ezz-Eldeen , M. Svendsen Benjamin Fe´ lix, Sophie A. Granier,
Bakry and S.Ismail, 2015. Prevalence of some Abera Geyid, Girum Taye and S. Rene, 2013.
food poisoning bacteria in local and imported retail Occurrence of Listeriaspp.in Retail Meat and Dairy
pork by-products in Egyptian markets. African J. Products in the Area of Addis Ababa, Ethiopia.
Microbiol Res., 9:1492-1498. 83.Selamawit, M., 2014. The Prevalence, Risk
73.Derra, F., S. Kalsmose, D.P. Monga, A. Mache, Factors, Public Health Implication And
C.A. Svedsen, B. Félix, S.A. Granier, A. Geyid, G. Antibiogram Of Listeria Monocytogenes, In Sheep
Taye and R.S. Hendriksen, 2013. Occurrence of Meat Collected From Municipal Abattoir And
Listeria spp. in retail meat and dairy products in the Butcher Shops In Addis Ababa.
area of Addis Ababa, Ethiopia. Foodborne Path. 84.Fredericks, P., M. Britz, R. Eastman, J. Carr and K.
Dis., 10:577-579. Bateman, 2015. Listerial brainstem encephalitis--
74.El Marnissi, B., L. Bennani, N. Cohen, A. Lalami treatable, but easily missed. South African Med. J.,
and R. Belkhou, 2013. Presence of Listeria 105:17-20.
monocytogenes in raw milk and traditional dairy 85.Painter, J. and L. Slutsker, 2007. Listeriosis in
products marketed in the north-central region of humans, listeriosis and Food Safety, 3 ed. Eds.
Morocco. African J. Food Sci., 7:87-91. 86.Goulet, V., L. King L, V. V. Vaillant and H. de
75.Bouayad, L. and T. Hamdi, 2012. Prevalence of Valk, 2013. What is the incubation Dara et al.13
Listeria spp. in ready to eat foods (RTE) from period for listeriosis? BMC Infect. Dis.
Algiers (Algeria). Food Control, 23(2):397- 13:11.doi:10.1186/1471-2334-13-11.
399.68803607 87.Romanolo, K., L. Gorski, S. Wang and C. Lauzon,
76. Gebretsadik, S., K. Tesfu , A. Haile, H. Kahsay 2015. Rapid identification and classification of
and K. Nigatu, 2010. Isolation and characterization Listeria spp. and serotype assignment of Listeria
of Listeria monocytogenesand otherListeriaspecies monocytogenes using fourier transform-infrared

76
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78
99.Leong, D., A. Alvarez-Ordonez and K. Jordan,
spectroscopy and artificial neural network analysis. 2014. Monitoring occurrence and persistence of
PloS one, 10: e0143425. Listeria monocytogenes in foods and food
88.European Centre for Diseases Prevention and processing environments in the Republic of
Control (ECDC), 2017. Facts about listeriosis Ireland. Front. Microbiol. n 5
Stockholm: ECDC, Available from: doi:10.3389/fmicb.2014.00436.
https://ecdc.europa.eu/en/listeriosis/facts. 100. Lamonaco, S., L. Decastelli, N. Nucera, S.
89.Centre for Disease Control and Prevention (CDC), Gallina, B. Manilla, D. Bianchi and T. Civera,
2017. Listeria (Listeriosis) Atlanta (USA). 2009. Association between a case study of
Available from: asymptomatic ovine listerial mastitis and the
https://www.cdc.gov/listeria/index.html. contamination of soft cheese and cheese processing
90.World Health Organization (WHO), 2017. Listeria environment with Listeria monocytogenesin
infections Geneva, Switzerland. Portugal. Foodborne Pathogens and Disease, 6:
91.Nature microbiology, 2016 569e575.
92.Ruppitsch, W., A. Pietzka, K. Prior, S. Bletz , H.L. 101. Pulse Net USA, 2009. International Standard
Fernandez and F. Allerberger, 2015 . Defining and PulseNet protocol. Available at:
Evaluating a Core Genome Multilocus Sequence http://www.cdc.gov/pulsenet/pathogens/listeria.htm
Typing Scheme for Whole-Genome Sequence- lAccessed 23/4/2014.
Based Typing of Listeria monocytogenes. J Clin 102. Muhterem-Uyar, M., M. Dalmasso, A.S.
Microbiol, 53(9):2869-76. Bolocan, M. Hernandez, A.E. Kapetanakou, T.
93.Moosavy, M.R., E. Saber, M. Ehsan and B. Kuthta, S.G. Manios, B. Melero, J. Minarovičová,
Fahimeh, 2014 . Isolation of Listeria A.I. Nicolau, J. Rovira, P. Skandamis, K. Jordan,
monocytogenes from milks used for Iranian D. Rodríguez-Lázaro, B. Stessl and M. Wagner,
traditional cheese in Lighvan cheese factories. 2015. Environmental sampling for Listeria
Anals of Agricultural and Environmental Medicine, monocytogenes control in food processing
21(4):728729. facilities reveals three contamination scenarios.
94.Dalmasso ,M., 2014. Comparison of polymerase Food Control, 51:94-107.
chain reaction methods and plating for analysis of 103. Dalmasso, M. and K. Jordan, 2013. Process
enriched cultures of Listeria monocytogenes environment sampling can help to reduce the
when using the ISO11290-1 method. J. Microbiol. occurrence of Listeria monocytogenes in food
Methods, 98:8-14. processing facilities. Irish J. Agric. Food Res.,
95.Rossmanith ,P., P. Mester, M. Wagner and D. 52:93-100.
Schoder ,2010. Demonstration of the effective 104. Haase, J., X. Didelot, M. Lecuit, H. Korkeala
performance of a combined enrichment /real-time and M. Achtman, 2014. The ubiquitous nature of
PCR method targeting the prfA gene of Listeria Listeria monocytogenes clones: a large‐scale
monocytogenes by testing fresh naturally Multilocus Sequence Typing study. Environ.
contaminated acid curd cheese. Lett.Appl. Mi Microbiol, 16:405-416.
crobiol, 51:480-484. 105. Müller, A., K. Rychli, M. Muhterem-Uyar, A.
96.Latorre, A.A., A.K. Pradhan, J.A.S. Van Kessel, Zaiser, B. Stessl, C.M. Guinane, P.D. Cotter,
J.S. Karns, K.J. Boor, D.H. Rice and Y.H. M.Wagner and S. Schmitz-Esser, 2013. Tn6188 -
Schukken, 2011.Quantitative risk assessment of A Novel Transposon in Listeria monocytogenes
listeriosis due to consumption of raw milk. J Food Responsible for Tolerance to Benzalkonium
Prot, 74:1268-1281. Chloride. PLoS ONE, 8(10):e76835.
97.Valimaa, A.L., A. Tilsala-Timisjarvi and E. 106. Ryan, S., M. Begley, C. Hill and C.G. Gahan,
Virtanen, 2015. Rapid detection and identification 2010. A five-gene stress survival islet (SSI-1) that
methods for Listeria monocytogenes in the food contributes to the growth of Listeria
chain –A review. Food Control, 55:103-114. monocytogenesin suboptimal conditions. J. Appl.
98.Morobe, I., B. Gashe , C. Obi , M. Nyila and M. Microbiol 109:984-95 doi:10.1111/j.1365-
Matsheka, 2012. Molecular Characterization and 2672.2010.04726.x.
Serotyping of Listeria monocytogenes with a 107. Cotter, P., L. Draper, E. Lawton, K. Daly, D.
Focus on Food Safety and Disease Prevention. Groeger, P. Casey, R. Ross and C. Hill, 2008.
INTECH Open Access Publisher. Listeriolysin S, a novel peptide haemolysin
associated with a subset of lineage I Listeria
monocytogenes. PLoS Pathog, 4(9):e1000144.
77
 Int. J. Adv. Res. Biol. Sci. (2019). 6(10): 64-78

108. Stess, B., M. Fricker, E. Fox, R. Karpiskova, growth limits of Listeria monocytogenes in milk,
K. Demerova, K. Jordan, M. Ehling-Schulz and M. broth and cheese. J. Appl. Microbiol, 109:1790-
Wagner, 2014. Collaborative survey on the 1799.
colonization of different types of cheeseprocessing 113. De Castro, V., J. Escudero, J. Rodriguez, N.
facilities with Listeria monocytogenes. Foodborne Muniozguren, J. Uribarri , D. Saez and J. Vazquez,
Path. Dis., 11:8-14. 2012. Listeriosis outbreak caused by Latin-style
109. Gilmour, M., M. Graham, G. Van Domselaar, fresh cheese, Bizkaia, Spain, August 2012. Euro
S. Tyler, H. Kent, K. Trout-Yakel, O. Larios, V. surveillance: European Communicable Disease
Allen, B. Lee and C. Nadon, 2010. High- Bulletin, 17(42).
throughput genome sequencing of two Listeria 114. Jamali ,H., B. Radmehr and K.L. Thong,
monocytogenesclinical isolates during a large 2013. Prevalence, characterisation and
foodborne outbreak. BMC Genom, 11:120 doi: antimicrobial resistance of Listeria species and
10.1186/1471-2164-11-120. Listeria monocytogenes isolates from raw milk in
110. Rychli, K., A. Müller, A. Zaiser, D. Schoder, farm bulk tanks. Food Control, 34(1): 121-125.
F. Allerberger, M. Wagner and S. Scmitz-Esser, 115. Olaniran, A.O., S.B. Nzimande and N.G.
2014. Genome sequencing of Listeria Mkize, 2015. Antimicrobial resistance and
monocytogenes ―Quargel" listeriosis outbreak virulence signatures of Listeria and Aeromonas
strains reveals two different strains with distinct in species recovered from treated wastewater effluent
vitro virulence potential. PloS one 9(2):e89964 and receiving surface water in Durban, South
doi:10.1371/journal.pone.0089964. Africa. BMC microbiology, 15(1): 234.
111. Schvartzman, M.S., C. Belessi, F. Butler, 116. Rajkovic, A., N. Smigic and F. Devlieghere,
P.N. Skandamis and K.N. Jordan, 2011. Effect of 2010.Contemporary strategies in combating
pH and water activity on the growth limits of microbial contamination in food chain.
Listeria monocytogenes in a cheese matrix at International Journal of Food Microbiology, 141:
two contamination levels. J. Food Prot., 74:1805- 29-42.
1813. 117. Pal, M., 2007. Zoonoses. Second edition.
112. Schvartzman, M.S., X. Belessi , F. Butler, P. Satyam Publishers, Jaipur, India, 118-119
Skandamis and K. Jordan, 2010. Comparison of

Access this Article in Online

Website:
www.ijarbs.com

Subject:
Veterinary
Sciences
Quick Response Code
DOI:10.22192/ijarbs.2019.06.10.007

How to cite this article:

Enkeshe Loha Yada and Zenebech Katimar Anato. (2019). A Review on Listeria monocytogenes in Food of
Animal Origin. Int. J. Adv. Res. Biol. Sci. 6(10): 64-78.
DOI: http://dx.doi.org/10.22192/ijarbs.2019.06.10.007

78