Implication of Corynebacterium species in food’s contamination

Abstract

Corynebacterium spp. are part of the human microbiota. Recently, species of this genus are
increasingly implicated in different types of infections especially in immunocompromized
and hospitalized patients. The significance of the presence of the genus Corynebacterium in
foods is not clearly established. These bacteria may be involved in spoilage or ripening of
cheese and meats. This review focused on different researches concerning the implication of
Corynebacterium species in food’s contamination.

Full text

416
Mini-review doi: 10.12980/jclm.4.2016J6-26 ©2016 by the Journal of Coastal Life Medicine. All rights reserved.
Implication of Corynebacterium species in food’s contamination
Sana Alibi
1,2 *
, Asma Ferjani
1
, Jalel Boukadida
1
1
UR12/SP34 Laboratory of Microbiology and Immunology, Universitary Hospital Farhat Hached Sousse, Tunisia
2
Faculty of Sciences of Bizerte, University of Carthage, Tunis, Tunisia
Journal of Coastal Life Medicine
2016; 4(5): 416-419
Journal of Coastal Life Medicine
*Corresponding author: Sana Alibi, UR12/SP34 Laboratory of Microbiology and
Immunology, Universitary Hospital Farhat Hached Sousse, Tunisia.
Tel: + 21698 980 610
Fax: +216 73 255900
E-mail: alibi_sana@hotmail.fr
The journal implements double-blind peer review practiced by specially invited
international editorial board members.
1. Introduction
The genus
Corynebacterium
represents one of the earliest
described bacterial genera. Recently, we can observe an increasing
number of publications describing different incidents of infections,
where species of
Corynebacterium
are isolated as the etiological
factor
[1-6]
. This genus was originally proposed for the causative
organism of
Corynebacterium diphtheriae
(Lehmann and Neumann,
1896) for diphtheria with the most important human-pathogenic
significance
[7-9]
. Strains of this species produce a strong exotoxin
and are responsible for causing diphtheria. Actually, the genus
Corynebacterium
comprises a broad range of additional important
different species with pathogenic significance including species
pathogenic for animals,
e.g.
Corynebacterium pseudotuberculosis
(
C. pseudotuberculosis
)
[10,11]
,
Corynebacterium kutscheri
[12,13]
,
Corynebacterium canis
[14]
and a very large group of saprophytic
species colonizing the skin and mucous membranes of man, which
may become the cause of serious infections in immunocomprmosed
and hospitalized patients.
The genus
Corynebacterium
includes also species unrelated
to the human organism,
e.g.
Corynebacterium glutamicum
(
C.
glutamicum
), producing L-glutamic acid and lysine, used in
biotechnological processes on the industrial scale and in genetic
studies
[15-17]
. However, the significance of the presence of the genus
Corynebacterium
in foods is not clearly established. These bacteria
may be involved in spoilage or ripening of cheese and meats. They
may also act as indicators of sanitation or hygienic quality. In this
work, we summarized the implication of
Corynebacterium
species
in food’s contamination.
2.
Corynebacterium
in milk
Together with the genera
Staphylococcus, Escherichia
and
Enterococcus
, members of the genus
Corynebacterium
represent
one of the most relevant mastitis-associated pathogens in
dairy farming
[18,19]
.
Corynebacterium
bovis
(
C. bovis
) and
Corynebacterium amycolatum
are frequently isolated from bovine
mammary glands
[20]
.
The lipophilic species
C. bovis
is frequently isolated from milk
samples in many dairy farms. It is associated with very mild forms
of mammary inflammation. Slightly increased somatic cell counts
in the milk are usually the only manifestations of these infections.
In a preliminary study, yield and composition of milk from 53
C. bovis
-infected quarters of 44 cows at four consecutive milkings
were compared with those of the contralateral uninfected quarters.
Differences between infected and uninfected quarters in milk, fat
and protein content were small and statistically non significant.
However, numbers of somatic cells were significantly higher in
ARTICLE INFO ABSTRACT
Corynebacterium
spp. are part of the human microbiota. Recently, species of this genus are
increasingly implicated in different types of infections especially in immunocompromized
and hospitalized patients. The significance of the presence of the genus
Corynebacterium
in
foods is not clearly established. These bacteria may be involved in spoilage or ripening of
cheese and meats. This review focused on different researches concerning the implication of
Corynebacterium
species in food’s contamination.
Article history:
Received 29 Jan 2016
Received in revised form 29 Feb 2016
Accepted 1 Apr 2016
Available online 17 May 2016
Keywords:
Corynebacterium
Food
Contamination
Spoilage
journal homepage: www.jclmm.com

Sana Alibi/Journal of Coastal Life Medicine 2016; 4(5): 416-419
417
infected than in uninfected quarters
[21]
. In agreement with previous
work, this preliminary trial with uninfected quarters revealed that
front quarters produced less milk than rear quarters. Composition
of milk from front and rear quarters was similar. Also, as expected,
milk produced after a longer milking interval was greater in volume
but lower in fat and protein content than that produced after a shorter
interval. In the same work, milk yields from
C. bovis
infected and
uninfected quarters were compared. There was a small but non-
significant reduction in yield from infected quarters
[22]
. This is
in agreement with Brooks who found no significant effect of
experimental infection with
C. bovis
on milk production
[23]
.
In addition to
C. bovis
, a new lipophilic oxidative species,
Corynebacterium mastitidis
, has been recognized and described
from the milk of sheep
[24]
. In another work, the same team isolated
a new species,
Corynebacterium
camporealensis
, from sheep
milk associated with subclinical mastitis
[25,26]
. Fermentative
nonlipophilic corynebacteria are much less often found in mastitic
milk.
Corynebacterium ulcerans
has been described as a cause of
bovine mastitis with a potential risk for humans, but its pathogenic
significance has remained unclear
[27-29]
. In addition to caseous
lymphadenitis,
C. pseudotuberculosis
was isolated as a causative
agent of cows and mastitis of sheep. Aroch
et al
.
[30]
noted a decrease
in milk production and considerable increase in the somatic cell
count in the mastitic cows. Several studies suggested that the
housefly plays an important role in harbouring and disseminating
C.
pseudotuberculosis
in dairy herds in Israel
[31,32]
.
Two other species,
Corynebacterium amycolatum
and
Corynebacterium minutissimum
, are known to be associated with
mastitis of dairy cows
[28]
. In a published work, Wiertz
et al
.
[33]
described 2 new species:
Corynebacterium frankenforstense
belonging to Frankenforst, the name of the experimental farm,
isolated from a bulk milk tank of a dairy farm in Germany and
Corynebacterium
lactis
isolated from raw cow milk produced in
Germany.
3.
Corynebacterium
in cheese
Smear-ripened cheeses, such as Munster, Livarot, Maroilles,
Limburger, and Tilsit, are characterized by the presence of a
complex flora on the surface, comprising many species of yeasts
and bacteria. The surface flora has a strong effect on the flavor,
texture, and appearance of these cheeses. Yeasts dominate during
the early stages of ripening because they are acid tolerant and salt
tolerant
[34]
. They increase the pH of the cheese curd by assimilating
lactate and producing alkaline compounds, and they also liberate
growth factors, thereby favoring the growth of bacterial species.
At the end of ripening, the bacteria are dominant, especially the
bacteria belonging to the genera
Corynebacterium
,
Brevibacterium
,
Arthrobacter
, and
Micrococcus
[35-39]
. The main sources of surface
microorganisms are milk, ripening environment, and inoculation of
cheese by the use of defined surface cultures or of the so-called “old-
young” smearing procedure, in which young cheeses are inoculated
with microorganisms from mature cheeses
[37]
.
Corynebacterium casei
[40-42]
, and
Corynebacterium
mooreparkense
[subsequently shown to be
Corynebacterium
variabile
(
C.
variabile
)]
[43-45]
, were identified in smeared cheese.
Graviera is the most popular traditional Greek hard cooked
cheese
[46]
. Several varieties are produced in different regions of
Greece from ewes’, ewes’ mixed with goats’, or cows’ milk, and
three of them produced in the islands of Crete and Naxos and the
mountain area of Agrafa have protected designation of origin status.
Recently, Samelis
et al.
[47]
evaluated the microbiological quality
and the safety of Graviera cheeses traditionally manufactured at
semi-industrial plant scale from thermized milk with addition of a
product-specific commercial starter culture and isolated five strains
of
Corynebacterium
sp. and
C. variabile
.
The importance of the bacterial flora for the ripening process
has been emphasized, but few studies on the identification of the
species present in red smear cheeses have been published. In 1997,
Valdés-Stauber
et al
.
[39]
focused on the species of coryneform
bacteria and yeasts which occur on the surface of ripe brick cheeses
and noted that
Arthrobacter nicotianae
,
Brevibacterium linens
,
Corynebacterium ammoniagenes, C. variabile
and
Rhodococcus
fascians
were found in significant numbers with a large number
of coryneform isolates that could not be identified to the species
level.
Corynebacterium
spp. produce extracellular enzymes that are
important for the development of the characteristic flavors, colors,
aromas and textures of these cheeses
[39]
.
4.
Corynebacterium
in vegetables
Corynebacterium
species have been isolated as a causative
agent for the spoilage in field and stored vegetables and fruits.
Corynebacterium michiganense
was identified in vascular
wilt, canker, leaf and fruit spot on tomatoes.
Corynebacterium
nebraskense
may cause leaf spot and blight and wilt corn.
Corynebacterium sepedonicum
was isolated from tuber rot of white
potatoes. Also,
Corynebacterium flaccumaciens
was associated with
bacterial wilt of beans
[48]
. Moreover,
Corynebacterium
spp
.
has been
isolated from frozen peas, beans and corns
[49]
and was responsible
for spoilage in frozen vegetables in Botswana
[50]
.
5.
Corynebacterium
in meats
Corynebacterium
spp
.
could grow at 5
°
C, indicating that species
of this genus are psychrophilic. Psychrophilic
Corynebacterium
species have been isolated from refrigerated food. In a survey done
in England, large numbers of psychrophilic
Corynebacterium
species
were recovered from feathers and feet of poultry during processing.
In recent report in Nigeria,
Corynebacterium
spp
.
were isolated from
poultry farms suggesting that the flock of birds and the consumers
of the eggs and meat from the chickens are at risk of bacterial
infection
[51,52]
. In previous studies,
Corynebacterium
was isolated
from bacon
[53]
. Also,
Corynebacterium
spp
.
were isolated from
poultry and eggs
[54]
. In fact,
Brevibacterium
and
Corynebacterium
were the most prevalent isolates from turkey giblets
[54]
. Recently,
Corynebacterium
spp
.
was isolated from retail mouton and lamb in
South Africa
[55]
.
6.
Corynebacterium
in sea foods
Corynebacterium
atrinae
was isolated from the gastro intestinal
tract of a pen shell.
Corynebacterium maris
sp. nov., a marine
bacterium, was isolated from the mucus of the coral
Fungia
granulosa
[56]
.
Corynebacterium
aquaticum
, originally found in both
distilled water and natural fresh waters, has been reported to cause
disease in some immunocompromised patients
[57-59]
, and it was
isolated from brain tissues of fish exhibiting pronounced bilateral

Sana Alibi/Journal of Coastal Life Medicine 2016; 4(5): 416-419
418
exophthalmia. Personnel involved in culturing fish should be made
aware of the pathogenic capability exhibited by
Corynebacterium
aquaticum
for mammals.
7.
Corynebacterium
in an alcohol fermentation starter
Shin
et al
.
[60]
described a novel Gram-positive, strictly aerobic and
non-motile bacterial strain
Corynebacterium nuruki
isolated from an
alcohol fermentation starter of traditional Korean wine.
8.
Corynebacterium
in food industry
In addition to their implication in food spoilage and contamination,
Corynebacterium
spp
.
were interestingly implicated in food industry
especially
C. glutamicum
.
C. glutamicum
is a very important
fermentative bacteria that is most widely known for its role in the
production of monosodium glutamate and amino-acids. Discovered
in 1957 in Japan as a natural producer of glutamic acid,
C.
glutamicum
is a Gram-positive, facultatively anaerobic, heterotrophic
bacterium with an irregular rod shape in a V-formation. It is non-
pathogenic and is found in soil, animal feces, fruits and vegetables.
Though it was originally isolated for its ability to produce massive
amounts of glutamic acid,
C. glutamicum
and its closely related
organisms have been developed for the production of most of the
biogene amino acids, nucleotides, and vitamins
[61]
.
9. Conclusion
In conclusion, the implication of
Corynebacterium
species as food
contaminant species is undertaken. However, this bacterium is a
serious threat to a safe food supply. It may be present in a variety of
consumed food and can be transmitted to human causing diseases.
There are several precautions that must be taken to insure that food is
not contaminated, that processing procedures are sufficient and that
storage conditions don’t allow
Corynebacterium
growth. As always,
good manufacturing practices and sanitation decrease the risk of a
foodborne illness becoming a serious health problem.
Conflict of interest statement
We declare that we have no conflict of interest.
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