Public Health Significance of Listeria monocytogenes in Milk and Milk Products: An Overview

Abstract

Milk and milk products serve as important source of many disease producing microbes including Listeria monocytogenes, which is a Gram-positive, motile, psychotropic bacterium, and is the principal cause of listeriosis in humans and in a wide variety of animals including birds. The disease occurs in sporadic as well as in epidemic form, following the ingestion of food contaminated by this organism. In the world, it is becoming an important food-borne bacterial disease, with low incidence but high case fatality rate. L. monocytogenes primarily affects older, pregnant women, newborns, and adults with weakened immune systems; and it has been recovered from the soil, dust, water, sewage, decaying vegetation, etc. Raw or inadequately pasteurized milk (or milk contaminated post-pasteurization), soft cheeses, ice cream and other dairy products are important sources of L. monocytogenes in humans. The disease has two forms, one febrile gastroenteritis and other inva-sive systemic disease. The control of Listeria in foods relies largely on a HACCP approach and the establishment of effective critical control points in the process. As milk and milk products are important vehicles of L. monocytogenes and clear risk factors, it is emphasized that people susceptible for acquiring listeriosis should not consume unpasteurized milk and milk products.

Full text

J. Vet. Pub. Hlth., 2014, 12 (1): 01-05
JOURNAL OF
VETERINARY PUBLIC
HEALTH
Public Health Significance of Listeria monocytogenes in Milk
and Milk Products: An Overview
M. Pal and H. Awel
Department of Microbiology, Immunology and Public Health, College of Veterinary Medicine and
Agriculture, Addis Ababa University, P.O. Box No. 34, Debre Zeit, Ethiopia
(Received 01.07.2013; accepted 17.06.2014)
ABSTRACT
Milk and milk products serve as important source of many disease producing microbes including Listeria
monocytogenes, which is a Gram-positive, motile, psychotropic bacterium, and is the principal cause of listeriosis
in humans and in a wide variety of animals including birds. The disease occurs in sporadic as well as in
epidemic form, following the ingestion of food contaminated by this organism. In the world, it is becoming an
important food-borne bacterial disease, with low incidence but high case fatality rate. L. monocytogenes prima-
rily affects older, pregnant women, newborns, and adults with weakened immune systems; and it has been
recovered from the soil, dust, water, sewage, decaying vegetation, etc. Raw or inadequately pasteurized milk
(or milk contaminated post-pasteurization), soft cheeses, ice cream and other dairy products are important
sources of L. monocytogenes in humans. The disease has two forms, one febrile gastroenteritis and other inva-
sive systemic disease. The control of Listeria in foods relies largely on a HACCP approach and the establish-
ment of effective critical control points in the process. As milk and milk products are important vehicles of L.
monocytogenes and clear risk factors, it is emphasized that people susceptible for acquiring listeriosis should
not consume unpasteurized milk and milk products.
Keywords: HACCP, Listeria monocytogenes, milk and milk products, pasteurization, public health.
Introduction
Milk is supposed to constitute a complex ecosystem
for various microorganisms including bacteria. Milk
products like cheese, ice cream and curd are widely
consumed and market for them has existed in many parts
of the world for many generations. Raw milk and other
dairy products are consumed by all age groups, including
those populations at risk for contracting listeriosis (Pal
et al., 2012 a). The disease primarily affects older, pregnant
women, newborns, and adults with weakened immune
systems. However, rarely, persons without these risk
factors can also be affected. Among the different species
of the genus Listeria, L. monocytogenes has been known to
cause listeriosis in humans and animals (Schukken et al.,
2003 and Pal, 2007).
L. monocytogenes emergence as a food borne pathogen
dates from 1980, with the occurrence of many outbreaks
and sporadic cases of listeriosis associated with the
consumption of contaminated foods. The increase in
consumption of many types of ready-to-eat foods that
are stored for fairly long periods of time, and the fact
that many of these foods are consumed without properly
reheating or by microwave heating, has given an edge
for this pathogen to cause the disease. Any temperature
abuse, even for a short time, can accelerate the growth
rate. It is quite clear that many of the above conditions
have given an advantage to L. monocytogenes to become
a newly emerging food borne pathogen in many
countries (Bibek and Arun, 2008). The present
communication delineates the public health significance
of Listeria monocyogenes in milk and milkproducts.
Etiology
Listeriosis is a serious illness caused by eating food
contaminated with the bacterium Listeria, which is a
Gram-positive, psychotropic, facultative anaerobic, non-
sporulating, motile, small rod (Pal, 2007). It displays
characteristic tumbling motility that is facilitated by the
presence of peritrichous flagella. Motility is temperature
dependent, showing high motility at 20-30°C when
flagellar expression is maximum. Out of the ten species of
genus Listeria (L. monocytogenes, L. ivanovii, L. seeligeri, L.
*Corresponding author: palmahendra2@gmail.com

innocua, L. welshimeri , L. grayi, L. marthi, L. rocourtiae, L.
fleischmannii and L. weihenstephanensis), L. monocytogenes
and L. ivanovii are pathogenic species to humans and
animals although human cases of L. ivanovii infection are
rare (Bibek and Arun, 2008, Chakraborty and Hain, 2013).
Epidemiology
Reservoirs and Risk factors
Listeria species are widespread in nature and live
naturally in plants and soil environments. It can grow in
a wide range of temperature and pH, and they are
relatively resistant to freezing, drying, and high salt
concentration (Bhilegaonkar et al., 2001). These
adaptabilities enable Listeria to grow in refrigerated raw
milk and in low quality silage with a pH>4.5. At high
bacterial concentrations, L. monocytogenes can survive
minimum HTST pasteurization (Bunning et al., 1988).
L. monocytogenes has been recovered from dust, soil,
water, sewage, decaying vegetation, at least 42 species of
wild and domestic mammals, and 17 avian species,
crustaceans, pond trout, ticks, and flies. Among food
sources milk and milk products, and uncooked vegetables,
fish and shellfish, ready-to-eat meat products, ground beef,
and poultry have all been found to contain the organism
(Gellin and Broom, 2001). In addition, a human reservoir
is suggested by isolation of the organism from human feces
at rates ranging from 6% to 16% of the population at any
given time (Lamont and Postlethwaite, 2001)
Modes of Transmission
The most common route of infection of humans is
consumption of foods contaminated by L. monocytogenes
(Pal, 2007). Inadequately pasteurized milk (or milk
contaminated post-pasteurization), soft cheeses, ice
cream and other dairy products also are important
sources of L. monocytogenes (MacDonald et al., 2005; Pal
et al., 2012a). Milk and milk products are considered as
risk foodstuffs for L. monocytogenes (Pal et al., 2012b).
Pregnant women can transmit the infection to their
unborn fetuses in utero (through hematogenous spread)
or during birth (Siegman-Igra et al., 2002).
Prevalence
L. monocytogenes has been reported several times from
raw milk, in different countries; in USA, in 1987 (4.2%),
in 1992 (4.1%), in 1997 (4.6%); in Canada, in 1988 (1.3%,
and 5.4%), and in 1998 (2.7%); in South Africa, in 1990
(5.2%); in Ireland, in 1992 (4.9%) and in England and
Wales (5.1%) (Siegman-Igra et al., 2002). The source of L.
monocytogenes in raw milk is mostly the gastrointestinal
tract of animals and the environment, skin of the teats,
in particular shedding of Listeria into milk due to mastitis
(O’Donnell, 1995). In cows with mastitis, L. monocytogenes
may be shed at 10,000-20,000 cells per ml of milk, with
the appearance of the milk being normal and there being
no inflammation of the affected quarter. So that raw milk
collection has the potential of delivering L.monocytogenes
to the cheese making facility (Bunning et al., 1988).
Studies conducted in different countries have
demonstrated the presence of L. monocytogenes and other
Listeria species in milk (Table 1). Most reports concern
raw milk but there are few reports for pasteurized milk.
Population at risk
Healthy adults and children occasionally get infected
with L. monocytogenes, but they rarely become seriously
ill. The body’s defense against L. monocytogenes is called
“cell-mediated immunity” because it depends on our
cells, especially lymphocytes called “T-cells.” Therefore,
individuals whose cell-mediated immunity is suppressed
are more susceptible to the devastating effects of
listeriosis. Pregnant women naturally have a depressed
cell-mediated immune system. In addition, the systems
of fetuses and newborns are very immature and are
extremely susceptible to these types of infections (Richard
et al., 2008).
However, in most African countries, there are a few
reports on Listeria and listeriosis, when compared to the
Europe and USA. This could be associated with lack of
awareness of laboratory technicians or lack of diagnostic
facilities and limited resources together with the presence
of other disease epidemics that claim more priority than
listeriosis in developing countries including Ethiopia.
However, nowadays there are some reports on
prevalence of L.monocytogenes in different samples. For
example, in Ethiopia (Addis Ababa) study conducted in
2004 showed that over all prevalence of 32.6% Listeria
species out of the total 316 examined samples with high
prevalence of L. monocytogenes in ice cream (19.6%) (Molla
et al., 2004). Also, of the samples examined (391) in Addis
Ababa in 2010, 102 (26.1%) were found to be positive for
Listeria. L. monocytogenes was detected in 5.4% of the
samples analyzed. It was isolated mainly from raw milk
(13%) (Gebretsadik et al., 2010).
Outbreaks associated with milk and milk products
Milk and milk products are one of the most frequently
incriminated comodity in the listeriosis outbreaks across
the world. The first report of listeriosis from milf was
form USA in 1983 (Fleming et al., 1985). Various milk
products namely cheese (Azadian et al., 1989; Ries et al.,
1990; Gilot et al., 1997; Schoder, D. et al., 2003), curd/
yoghurt (Greenwood et al., m 1991), ice-cream (Ryser,
1999), butter (Lyytikainen et al., 1999; Ryser, 1999),
chocolate milk (Dalton et al., 1997) etc. have been
implicated in the listeriosis cases.
02 Pal et al.

Table 1. Prevalence of L. monocytogenes in raw milk samples overseas
Country/ Sample type No. of No.(%) positive Reference
region samples tested for L. monocytogenes
Asia
Japan Raw, farm bulk tank 120 1 (0.8) Takai et al. (1990)
India Raw Milk Bhilegaonkar et al. (1997)
Raw cow milk 5.8% Soni and Dubey (2013)
Europe
France Raw, bulk tanks 1459 2.4% Meyer-Broseta et al. (2002)
Scotland Raw, bulk tanks 180 7 (3.8) summer Fenlon and Wilson (1989)
180 0 (0) autumn
180 2 (1.0) winter <1 cell/ml
Turkey Raw 211 2 (0.9) Uraz and Yücel (1999)
UK Raw 610 101 (16.5) Food Standards Agency (2003)
Pasteurized 1413 0
North America
Canada Raw, from 455 6 (1.3) Farber et al. (1998
Ontario bulk tanks
USA Raw 124 15 (12.0) Fleming et al. (1985)
Raw 121 15 (12.0) Hayes et al. (2001)
Raw 650 27 (4.2) Lovett et al. (1987)
Tennessee Raw, bulk farm tanks 292 12 (4.1) Rohrbach et al. (1992)
Clinical spectrum
Febrile gastroenteritis
The exact mechanism of gastroenteritis is not known;
however, epidemiological study suggests that this form
is mostly associated with healthy individuals and the
infectious dose is in the range of 108-1010 cells of
L.monocytogenes (Bibek and Arun, 2008). Incubation
period of this type ranges from 9-48 h after ingestion of
contaminated item. Watery diarrhea (blood rarely
present in the stool), fever, chills, nausea and vomiting
are the main presenting feature (Lorber, 2005).
Invasive systemic disease
This form of disease is associated with
immunologically challenged populations. These groups
include pregnant women, unborn fetuses, infants, elderly
people with reduced immunity due to diseases, and
people taking special medications, such as steroids and
chemotherapeutic agents to treat cancer. The infective
dose in these people is considered to be about 100-1000
cells of L. monocytogenes (Bibek and Arun, 2008).
Persistent infection allows the bacterium to infect
central nervous system. It crosses blood brain barrier
causing inflammation of meninges and brain stem. In
pregnant women, it can pass through the placental barrier
infecting the fetus. Abortion and stillbirth follows. The
incubation period for invasive disease is about 2-6 weeks
before the symptoms are visible (Bibek and Arun, 2008).
Fever, myalgias, nausea, diarrhea, mild influenza-like
illness and CNS signs are the main presenting feature
(Lorber, 2005).
Diagnostic techniques
Conventional cultural method
The two-stage enrichment method for detection of L.
monocytogenes with isolation on PALCAM agar and
Oxford agar (ISO, 1996) are widely used.
The CAMP reaction is useful for identifying Listeria
species. This test uses horse blood agar and streaks of
hemolytic Staphylococcus aureus and Rodococcus equi in
combination with Listeria isolates. L. monocytogenes and
L. seeligeri hemolytic reactions are enhanced in the zone
influenced by the S. aureus streak, while the other species
remain non-hemolytic in this zone. In contrast, the
hemolytic reaction of L. ivanovii is enhanced in the zone
influenced by R. equi (Hitchins, 2002). For confirmed and
specification, different standard biochemical tests can be
used. The biochemical confirmatory tests can be done
by picking pure colonies and transferring into the
following biochemical media and broths. These are
motility test medium (motility), blood agar (haemolysis),
mannitol, rhamnose, galactose, xylose, Hippurate
hydrolysis and xylose broths for carbohydrate
fermentation testing (James et al., 2005).
Molecular methods
As molecular methods are accurate, sensitive and
Public health significance of Listeria in milk and milk products 03

specific, they are increasingly used in Identification of L.
monocytogenes form foods. Various molecular methods
used are DNA hybridization, polymerase chain reaction
and real time PCR (RT PCR). Among these, PCR and real
time PCR are now established methods for identification
of Listeria monocytogenes from other non virulent Listeria
spp. from foods. In the the first reported PCR for
identification of L. monocytogenes, the hly sequence
published by Mengaud et al. (1988) was used. The real-
time PCR is a very sensitive and quantitative method for
derection of pathogen and thus has emerged as most
important tool for L. monocytogenes detection and
quantitation in foods (Hein et al., 2001; Hough et al., 2002).
Prevention and control
The control of Listeria in foods relies largely on a
HACCP approach and the establishment of effective
critical control points in the process. The careful design
and layout of processing equipment in conjunction with
the implementation of regular, thorough cleaning
regimes of the processing environment can significantly
reduce the level of Listeria contamination in many
processed foods. However, because of its ubiquitous
nature it is virtually impossible to totally eliminate the
pathogen from many food products. Vulnerable
individuals, especially pregnant women, the elderly and
the immunosuppressed are advised to avoid consuming
unpasteurized dairy products to reduce the risk from
listeriosis (Pal, 2007 and Richard et al., 2008).
Early detection of a listeriosis outbreak and efficient
intervention are important in preventing the epidemic
from continuing. Typing of food isolates and comparison
with clinical isolates may also lead authorities to
contaminated food processing plants. However, in
addition to typing results, epidemiological evidence is
needed for the incrimination of a food or a food
processing plant (Lukinmaa et al., 2003).
Standards/legislation for the pasteurization of ice
cream/frozen desserts adapted in various countries has
an importance in reducing of listeriosis. These heat
processes are more severe than HTST pasteurization
because ingredients such as sugars, fat, emulsifiers and
stabilizers in these products protect L. monocytogenes from
heat, resulting in an increase in D-value (Richard et al.,
2008).
Conclusions
L. monocytogenes has gained recognition as a global
human pathogen because of the increasing incidence,
diagnosis of infections, and also, it is widespread in
nature and lives naturally in plants and soil environments
and has potential to introduce food plant. It can grow in
a wide range of temperature and pH. Milk and milk
products are important vehicles of L. monocytogenes,
regularly causing listeriosis outbreaks in different
countries of the world. The consumption of raw milk or
products made of raw milk has caused several listeriosis
outbreaks resulting in several hundred cases. Raw milk
and raw milk products are therefore, clear risk factors
and people that are susceptible for acquiring listeriosis
should not consume such products. Good manufacturing
and hygiene practices, particularly maintaining hygiene
of processing machines, are the keys in preventing
L.monocytogenes contamination. It is also equally
important to notice that products, which may be
subjected to post processing contamination, should be
properly reheated before consumption by highly
immunocompromised persons in order to eliminate
possible contamination. A food safety management
system based on the principles HACCP with regular
reviews should be developed and implemented in dairy
plant.
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