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Ifrj-2010-306
Ifrj-2010-306
Review Article
Salmonella: A foodborne pathogen
Pui, C. F., 1Wong, W. C., 1Chai, L. C., 1Tunung, R., 1Jeyaletchumi, P.,
1
Noor Hidayah, M. S., 1Ubong, A., 1Farinazleen, M. G., 2Cheah, Y.
K. and 1*Son, R.
Abstract: Salmonellosis continues to be a major public health problem worldwide. It also contributes to
negative economic impacts due to the cost of surveillance investigation, treatment and prevention of illness. As
such, research on Salmonella has gained great interest and concern from scientists. The purpose of this review is
to discuss the classification and nomenclature, characteristic, clinical manifestation, epidemiology, transmission
vehicles, antibiotic resistance and quorum sensing of Salmonella.
Keywords: Salmonella, clinical manifestation, epidemiology, transmission, antibiotic resistance, quorum
sensing
Introduction
There are 16 million annual cases of typhoid
fever, 1.3 billion cases of gastroenteritis and 3 million
deaths worldwide due to Salmonella (Bhunia, 2008).
In brief, Salmonella is facultative anaerobe, gramnegative flagellated rod-shaped bacterium which is
about 2-3 x 0.4-0.6 m in size (Yousef and Carlstrom,
2003; Montville and Matthews, 2008).
It is among the most commonly isolated
foodborne pathogens associated with fresh fruits
and vegetables. In recent years, the incidence of
foodborne outbreaks caused by the contamination of
fresh fruits and vegetables has increased and become
a great concern in industrialized countries. Outbreaks
of salmonellosis have been linked to a wide variety
of fresh fruits and vegetables including apple,
cantaloupe, alfalfa sprout, mango, lettuce, cilantro,
unpasteurized orange juice, tomato, melon, celery
and parsley (Pui et al., 2011b).
Classification and nomenclature
Historically Salmonella had been named based
on the original places of isolation such as Salmonella
London and Salmonella Indiana. This nomenclature
system was replaced by the classification based on
the susceptibility of isolates to different selected
bacteriophages which is also known as phage typing
(Bhunia, 2008). Phage typing is generally employed
when the origin and characteristic of an outbreak
must be determined by differentiating the isolates
of the same serotype. It is very reproducible when
*Corresponding author.
Email: son@putra.upm.edu.my
Tel: +603-89468361; Fax: +603-89423552
466
Pui, C. F., Wong, W. C., Chai, L. C., Tunung, R., Jeyaletchumi, P., Noor Hidayah, M. S., Ubong, A., Farinazleen, M. G.,
Cheah, Y. K. and Son, R.
467
arizonae
IIIa
Coldblooded
animals &
environment
diarizonae
IIIb
Coldblooded
animals &
environment
houtenae
IV
Coldb1ooded
animals &
environment
indica
VI
Coldblooded
animals &
environment
Salmonella
bongori
V (formerly)
Coldblooded
animals &
environment
+ (except
+
+
+
+
+
pullorum &
gallinarum)
Rod
Rod
Rod
Rod
Rod
Rod
0.7-1.5
0.7-1.5
0.7-1.5
0.7-1.5
0.7-1.5
0.7-1.5
2-5
2-5
2-5
2-5
2-5
2-5
Black colonies surrounded by a brown to black zone that casts a metallic sheen
Translucent amber to colourless colonies
Blue to blue-green colonies, mostly with black centers (H2S producers)
Colourless colonies on a pink background
Black-centered red colonies (H2S producers)
35-37
6.5-7.5
d
d
+
+
+
+
+
+
+
+
+
-
35-37
6.5-7.5
+
+
+
+
+
d
+
+
+
+
d
d
+
-
35-37
6.5-7.5
+
d
+
+
+
+
+
+
+
+
+
+
+
-
35-37
6.5-7.5
+
+
+
+
+
+
+
+
+
-
35-37
6.5-7.5
+
+
+
+
+
+
+
+
+
+
+
+
+
+
-
35-37
6.5-7.5
+
+
+
+
+
+
+
+
-
35-37
6.5-7.5
+
d
d
+
+
+
+
+
+
+
+
d
+
+
-
Rod
0.7-1.5
2-5
Note: +, more than 90% positive reactions; -, less than 10% positive reactions; d, different reactions given by different serovars
468
Pui, C. F., Wong, W. C., Chai, L. C., Tunung, R., Jeyaletchumi, P., Noor Hidayah, M. S., Ubong, A., Farinazleen, M. G.,
Cheah, Y. K. and Son, R.
al., 2002).
The main food involved in salmonellosis is
shown in Table 2. Disease surveillance reports
frequently identify poultry (chickens, turkeys, geese
and ducks) as the main vehicles in the salmonellosis
outbreak. Salmonella Pullorum and Salmonella
Gallinarum usually cause disease in poultry. Cox
and Pavic (2010) provided extensive overview on
poultry meat production associated with Salmonella
and discussed the approaches for the control of this
pathogen throughout the whole production chain as
poultry can be contaminated from breeder flocks,
hatchery environment, feed and litter as well as water
troughs in the pens. In Malaysia, Arumugaswamy et
al. (1995) reported 39.4% chicken portions, 35.3%
chicken liver and 44.4% chicken gizzard were
contaminated with Salmonella spp.
469
Country
United States
United States
United States
United States
United States
United States
United States
Austria
England
The Netherlands
Malaysia
China
Great Britain
Germany
Canada, Australia
Norway, Sweden
Singapore
Japan
France
Switzerland
Source
Black and red pepper
Frozen mamey fruit pulp
Shell eggs
Alfalfa sprouts
Cereal from Malt-O-Meal
Dry pet food
Peanut butter
Mixed salad
Kebab
Imported raw beef
Stall food
Cake/raw egg topping
Lettuce
Aniseed herbal tea
Shandong peanuts
Fish
Dried anchovy
Dried squid
Mont Dor cheese
Potato salad prepared by carrier
Serotype
Montevideo
Typhi
Enteritidis
Saintpaul
Agona
Schwarzengrund
Tennessee
Enteritidis PT21
Enteritidis PT1
Typhimurium PT104
Typhi
Enteritidis
Newport
Agona
Stanley
Livingstone
Typhimurium DT104L
Salmonella spp.
Salmonella spp.
Typhi
Number of cases
272
9
2,752
235
28
62
>288
85
195
165
171
197
>350
42
93
60
33
<453
14
10
Reference
CDC, 2010
CDC, 2010
CDC, 2010
CDC, 2010
CDC, 2010
CDC, 2010
Montville and Matthews, 2008
DAoust and Maurer, 2007
DAoust and Maurer, 2007
DAoust and Maurer, 2007
Nik and Sharifah, 2005
DAoust and Maurer, 2007
Montville and Matthews, 2008
DAoust and Maurer, 2007
DAoust and Maurer, 2007
DAoust and Maurer, 2007
Ling et al., 2002
Montville and Matthews, 2008
Colak et al., 2007
Gruner et al., 1997
470
Pui, C. F., Wong, W. C., Chai, L. C., Tunung, R., Jeyaletchumi, P., Noor Hidayah, M. S., Ubong, A., Farinazleen, M. G.,
Cheah, Y. K. and Son, R.
Lithuania
Turkey
Vietnam
Malaysia
Brazil
South India
Jordan
Malaysia
Albania
India
Malaysia
Malaysia
Sample/source
chicken
beef
poultry carcass
poultry viscera
pig
herd
chicken
pork
beef
lamb
slaughter house
seafood
Prevalence
86/190 (45.3%)
38/189 (20.1%)
0/127 (0%)
2/73 (2.7%)
43/804 (5.3%)
22/67 (32.8%)
276/515 (53.6%)
28/91 (30.8%)
13/78 (16.7%)
16/80 (20%)
75/105 (71.4%)
10/105 (9.5%)
chick egg
retail pork
chicken part
minced meat
ready-to-eat salad
raw vegetable
raw milk
raw poultry
cooked poultry
raw meat
cooked meat
turkey
quail
vegetable
faeces
caecum
dust
water
tulum cheese
pork
beef
chicken
shellfish
street food
fried chicken
kerabu jantung pisang
sambal fish
mix vegetable
chicken abattoir
egg
chicken, meat
selom
pegaga
kangkong
kesum
chicken meat sample
fish
crustacean
retail poultry
litter
poultry farm
chicken portion
chicken liver
chicken gizzard
cooked meat, chicken,
vegetable
satay
prawn
oriental shrimp paste
4/80 (5%)
13/500 (2.6%)
1/168 (0.6%)
0/45 (0%)
0/100 (0%)
0/78 (0%)
0/25 (0%)
24/134 (17.9%)
3/56 (5.4%)
8/101 (7.9%)
2/118 (1.7%)
1/3 (33.3%)
2/5 (40%)
3/38 (7.9%)
28/85 (32.9%)
12/52 (23.1%)
5/34 (14.7%)
1/10 (10%)
6/250 (2.4%)
32/50 (64%)
31/50 (62%)
16/30 (53.3%)
9/50 (18%)
12/129 (9.3%)
1/18 (5.6%)
3/5 (60.0%)
6/9 (66.7%)
2/5 (40.0%)
29/288 (10.1%)
38/492 (7.7%)
25/93 (26.9%)
16/43 (37.2%)
8/26 (30.8%)
8/25 (32%)
8/18 (44.4%)
30/461 (6.5%)
104/730 (14.3%)
48/276 (17.4%)
158/445 (35.5%)
8/40 (20.0%)
2/10 (20.0%)
13/33 (39.4%)
6/17 (35.3%)
8/18 (44.4%)
4/28 (14.3%)
14/60 (23.3%)
4/16 (25%)
2/19 (10.5%)
Predominant serotypes
Thompson
Reference
Dallal et al., 2010
Enteritidis
Anatum, Typhimurium
Enteritidis, Baibouknown
Enteritidis, Typhimurium
Enteritidis, Typhimurium
Enteritidis
Enteritidis, Typhimurium
Weltevreden, Agona, Senftenberg,
Albany
Enteritidis
Weltevreden, Typhi, Paratyphi B,
Mgulani, Typhimurium
Enteritidis, Muenchen, Kentucky,
Blockley
Blockley, Enteritidis, Chincol,
Muenchen, Agona
eggs. Asai et al. (2010) mentioned that cephalosporinand fluoroquinone-resistant strains of S. Choleraesuis
have been identified in swines in Taiwan and Thailand.
Apart from that, antibiogram testing by Singh et al.
(2010) revealed Salmonella isolates from chicken
eggs in marketing channels and poultry farms in
North India were resistant to bacitracin, colistin and
polymyxin-B.
Due to the use of antibiotics for the promotion
of growth and prevention of disease in food animals,
there is an increase of human salmonellosis cases
caused by foodborne MDR Salmonella nowadays
(Yang et al., 2010). This indiscriminate and
injudicious use of antibiotics in any setting especially
in food animals worldwide should be monitored
to reduce the transfer risk of MDR Salmonella to
humans (Zhao et al., 2003). Finally, there is a need of
continuous surveillance and sharing of antimicrobial
susceptibility data for Salmonella among countries
worldwide (de Oliveira et al., 2010) to ensure the
effectiveness of control programmes.
Quorum sensing
Quorum sensing, also known as cell-to-cell
communication, is the mechanism that involves
the bacteria synthesis, secretion and detection of
hormone-like molecules known as autoinducers
(Elvers and Park, 2002; Reading and Sperandio,
2006). Once the signal molecule achieves the critical
threshold concentration, bacteria sense its presence
and start the signalling cascade which results in
the changes of target gene expression (Gobbetti
et al., 2007). Traits under quorum-sensing control
include antibiotic biosynthesis, extracellular polymer
production, biosurfactant synthesis, bioluminescence,
sporulation, surface attachment as well as secretion
of nutrient sequestering compounds and virulence
factors (Nadell et al., 2008). An example of the
traits under quorum sensing is biofilm formation
by Salmonella Typhi and Salmonella Typhimurium
on plastic cutting board as reported by Pui et al.
(2011a).
Quorum sensing in Salmonella involves LuxS/
AI-2 system which is the most widespread quorum
sensing system. Jimenez-Gomez et al. (2007)
471
472
Pui, C. F., Wong, W. C., Chai, L. C., Tunung, R., Jeyaletchumi, P., Noor Hidayah, M. S., Ubong, A., Farinazleen, M. G.,
Cheah, Y. K. and Son, R.
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