Download Bacteria of the genus Aeromonas in different locations

RPCV (2006) 101 (557-558) 125-129
R E V I S TA P O R T U G U E S A
DE
CIÊNCIAS VETERINÁRIAS
Bacteria of the genus Aeromonas in different locations throughout
the process line of beef slaughtering
Bactérias do gênero Aeromonas em diferentes pontos do fluxograma
de abate bovino
O. D. Rossi Júnior*, L. A. Amaral, A. Nader Filho, R. P. Schocken-Iturrino
*
Faculdade de Ciências Agrárias e Veterinárias, Campus de Jaboticabal, UNESP, 14.884-900 - Jaboticabal - SP
Summary: To determine the occurrence and the population of
bacteria of the genus Aeromonas at different points in the flow
diagram for cattle slaughter at a plant with a high hygiene-sanitation level under permanent federal inspection, we investigated
products and locations along the slaughter flow diagram from
animal arrival to boned meat ready for commercialization. Of the
30 samples taken in each of the nine locations investigated, the
bacteria of genus Aeromonas were isolated in 20 (66.6%) of the
samples collected from the forequarter hide, in 19 (63.3%) of the
samples collected from the hindquarter, another 5 (16.6%) and 3
(10.0%) from the samples collected from the muscle surface tissue of the forequarter and hindquarter, respectively, in 6 (20.0%)
samples of boned meat, in 4 (13.3%) knife surfaces, in 1 (3.3%)
sample of the environment of the slaughtering room, and from 12
(40.0%) samples of the intestinal content. Aeromonas spp wasn’t
isolated from the still dry animal skin at the time of animal arrival
at the slaughterhouse. The following species were isolated:
Aeromonas hydrophila from 9 (3.3%) samples, Aeromonas caviae
from 59 (21.8%), and atypical forms from 35 (13.0%). The mean
populations detected were 1.1 x 10 CFU/cm2 and 3.1 x 10 CFU/cm2
on the fore and back carcass skin, respectively, 1.5 x 102 CFU/cm2
on the muscular surface of the fore carcass, and 1.4 x 10 CFU/g
in the intestinal content. The results obtained demonstrated that,
despite the high hygiene-sanitation level of the slaughterhousemeat processing plant, the meat may be contaminated with
Aeromonas bacteria as early as at the time when it is first processed.
Keywords: Aeromonas spp, A. hydrophila, A. caviae, beef
slaughter.
Resumo: Com o objetivo de verificar a ocorrência e a população
de bactérias do género Aeromonas em diferentes pontos do fluxograma de abate bovino, em estabelecimento de alto nível higiénico-sanitário, foram investigados produtos e locais do fluxograma
de abate, desde a chegada dos animais até a carne desossada e
pronta para comercialização. Das 30 amostras colhidas em cada
um dos nove pontos investigados, as bactérias do género
Aeromonas foram isoladas em 20 (66,6%) amostras da pele do
membro dianteiro, em 19 (63,3%) da pele do membro traseiro,
em 5 (16,6%) e em 3 (10,0%) da superfície muscular dos membros
dianteiro e traseiro, respectivamente, em 06 (20,0%) de carne
desossada, em 4 (13,3%) de superfície de facas, em 1 (3,3%) do
ambiente da sala de matança e em 12 (40,0%) do conteúdo
intestinal. Não foram isoladas Aeromonas sp. da pele dos animais ainda seca, no momento da chegada desses ao matadouro.
*Correspondence: [email protected]
As espécies isoladas foram Aeromonas hydrophila em 09 (3,3%)
amostras e Aeromonas caviae em 59 (21,8%), além de 35
(13,0%) atípicas. As populações médias encontradas foram de
1,1x10 UFC/cm2 e de 3,1x10 UFC/cm2 na pele dos membros
dianteiro e traseiro, respectivamente, de 1,5x102 UFC/cm2 na
superfície muscular do membro dianteiro e de 1,4x10 UFC/g no
conteúdo intestinal. Os resultados obtidos evidenciaram que,
apesar do elevado nível higiénico-sanitário do matadouro-frigorífico, as carnes podem ser contaminadas com bactérias do
género Aeromonas já a partir de sua obtenção.
Palavras-chave: Aeromonas spp, A. hydrophila, A. caviae,
abate bovino.
Introduction
The different species of the genus Aeromonas are
considered to be emergent pathogens and are held
responsible for the occurrence of diseases classified as
non-intestinal and gastroenteric (Ko and Chuang,
1995). At the non-intestinal level, meningitis (Ellison
and Mostow, 1984), arthritis (Dean and Post, 1967),
endocarditis (Davis et al., 1978), osteomyelitis (Lopez
et al., 1968), peritonitis (Janda et al., 1983; Nygard et
al., 1970), cutaneous infections (Joseph et al., 1979)
and ocular infections (Lee et al., 1997), among others,
have been attributed to the action of Aeromonas bacteria.
At the gastroenteric level, these bacteria are considered
to be responsible for diseases ranging from mild diarrhea to severe dysentery (Knochel, 1989).
These microorganisms are widely diffuse in the
environment (Cunliffe and Adcok, 1989), with water
and food being the possible routes of transmission to
man. There are reports of isolation from polluted
waters (Joseph et al., 1979; Neves et al., 1990), from
non-chlorinated waters (Krovacek et al., 1989), from
chlorinated waters (Kersters et al., 1995), and from
waters used for the most diverse purposes in the food
industry (Gill and Jones, 1995; Rossi Júnior et al.,
1996b).
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Rossi Júnior OD et al.
The occurrence of different Aeromonas species in
foods of animal origin, especially commercially
obtained meats, has been reported by several investigators in studies conducted in different parts of the
world (Majeed et al., 1989; Fathi and Moustafa, 1991;
Gill and Jones, 1995; Rossi Júnior et al., 1996a,b;
Yadav and Verma, 1998).
The objective of the present study was to determine
the occurrence and population of bacteria of the genus
Aeromonas at different points along the flow diagram
of cattle slaughter.
Material and methods
The study was conducted at a slaughterhouse-meat
processing plant in the State of São Paulo, where the
following samples were analyzed: still dry animal skin
surface at the time of arrival to the plant, skin surface
of the fore and back carcass, after the animal was
washed by aspersion, muscular surface of the fore and
hind carcass, boned meat ready for commercialization, knife surface, and intestinal content.
Surface samples were collected with sterilized swabs
from 20 cm2 areas and transported to the plant in test
tubes containing 4 ml 0.1 % peptone water, according
to the method recommended by Apha (2001).
The meat samples were collected in the form of fragments at one point in the boning room and intestinal
content samples in the entrails and tripe processing
section at the time of the opening of the digestive tract
for washing and preparation. For the collection of environmental samples in the slaughter room, Petri dishes
containing selective media for the genus under study
(dextrin-ampicillin agar and phenol red-starch-ampicillin agar) were left open for 15 minutes (Apha, 2001).
The samples were transported in styrofoam boxes
containing ice cubes and immediately processed in the
laboratory for bacterial isolation and counts. For
isolation, 25 g of the meat and intestinal content samples were obtained and homogenized in a Stomacher‚
apparatus with 225 ml trypticase-soy broth (TSB) supplemented with ampicillin (Sigma – A9393) at the concentration of 30 mg/liter. The swabs and the peptone
water used for transport were poured into test tubes
containing 20 ml of the selective enrichment broth.
After incubation at 28 0C for 24 hours, the selective
enrichment cultures were streaked on dishes containing
phenol red-starch-ampicillin agar (Palumbo et al.,
1985) and dextrin-ampicillin agar (Havelaar and Vonk,
1988).
The dishes were incubated at 28 ºC for 24 hours and
examined for the presence of large colonies (3-5 mm)
surrounded by a yellow halo caused by the hydrolysis
of starch or dextrin, characteristic of the genus
Aeromonas. Up to five colonies were streaked in tubes
containing trypticase-soy agar (TCA) and tested for
motility, oxidase, catalase and resistance to the vibrio126
RPCV (2006) 101 (557-558) 125-129
static agent O/129 (2,4-diamine-6,7–diisopropylpteridine) according to the characterization scheme adopted
by Popoff (1984), Neves et al. (1990) and Hudson e
Lacy (1991). The species were characterized according
to the scheme of Popoff (1984) and using some other
tests recommended by Buchanan and Palumbo (1985).
The strains that showed a reaction differing from the
classification of Popoff (1984) in only one biochemical
test were considered atypical, as indicated by Majeed
et al. (1989).
Counts were performed in phenol red-starch-ampicillin by spreading on the surface of 0.2 ml volumes of
each sample collected from the surface, or by 1/10
dilution in the case of solid samples. Characteristic
colonies were counted and up to five colonies per dish
were tested for genus confirmation.
Results and discussion
Data concerning the frequency of isolation from the
various sample categories analyzed and the species
detected are presented in Table 1.
Bacteria of the genus Aeromonas were not isolated
from the dry skin surface of the animals at the time of
their arrival at the plant. These results suggest that,
when animals arrive at the plant, their outer body surface does not represent a source of significant contamination of bovine meat with Aeromonas microorganisms. On the other hand, the presence of these
microorganisms in a high percentage of samples from
the skin surface of the forequarter (66.6%) and
hindquarter (63.3%) after contact with water suggests
the possible role of water as a source of contamination, as discussed by Jindal et al. (1993) and Häninnen
and Siitonen (1995).
The lack of literature data concerning the study of
the presence of Aeromonas spp on the skin surface of
beef cattle impairs a comparative analysis with the
findings of the present study. However, on the basis of
the results obtained, we may conclude that the animal
skin, after washing, may become an important source
of meat contamination acting during the different
phases of slaughtering. With respect to the other possible sources of contamination, Table 1 shows that
Aeromonas was isolated from a significant number of
intestinal content samples (12/40.0%) and from 4
(13.3%) knife surface samples. The number of isolations from the intestinal content (12/40%) was higher
than that reported by Gray (1984) and Gray and
Stickler (1989) in England, by Abbey and Etang
(1988) in Nigeria and by Jindal et al. (1993) in India,
who detected Aeromonas in 21.1%, 4.6%, 2.86% and
10.0% of cattle feces samples, respectively. These
investigators refer that the occurrence of Aeromonas
in the digestive tract of animals depends on the exposure of the latter to water sources containing the
microorganism and that carcass contamination with
Rossi Júnior OD et al.
RPCV (2006) 101 (557-558) 125-129
Table 1 - Total samples analyzed and number and percentage of positives for each one of the species of the bacteria of the genus
Aeromonas identified in each type of samples collected at different locations throughout the beef slaughtering process line
Number of samples
Type of sample
Analyzed
Positives(%)
Aeromonas spp
Atypical
Aeromonas
A. hydrophila A. caviae
Dry hide surfaces – animals upon arrival
30
00
001(0,0)2
00(0,0)
00(0,0)
Surface of forequarter hide – after aspersion bath
30
20(66,6)
03(10,0)
17(56,6)
10(33,3)
Surface of hindquarter hide – after aspersion bath
30
19(63,3)
00(0,0)
17(56,6)
11(36,6)
Surface of muscle tissue forequarter
30
05(16,6)
01(3,3)
05(16,6)
01(3,3)
Surface of muscle tissue hindquarter
30
03(10,0)
01(3,3)
01(3,3)
03(10,0)
Deboned meat – commercial cuts
30
06(20,0)
02(6,6)
05(16,6)
03(10,0)
Surface of knives
30
04(13,3)
01(3,3)
03(10,0)
04(13,3)
Slaughter room area
30
01(3,3)
00(0,0)
01(3,3)
00(0,0)
Intestinal content
30
12(40,0)
01(3,3)
10(33,3)
03(10,0)
270
70(25,9)
09(3,3)
59(21,8)
35(13,0)
TOTAL
1
2
Number of samples in which the specie was found to be isolated in.
Percentage in relation to the total number of samples analyzed in each type.
intestinal content and transfer of the contaminants
between carcasses by cross-contamination during processing cannot be overlooked.
The knives used in the different procedures of cattle
slaughter are known to be easily contaminated from the
skin surface, gastrointestinal contents, water and other
sources, thus representing an additional vehicle of contamination. The presence of the genus Aeromonas in
equipment, developing on organic matter residues on
the surface of poorly cleaned surfaces has been previously demonstrated by Gill and Jones (1995).
Table 1 also provides information about the isolation
of bacteria of the genus Aeromonas from the muscle
surface of both the forequarter (05/16.6%) and hindequarter (03/10.0%) and from the meat (06/20.0%)
obtained in the boning room. Most of the studies concerning the presence of Aeromonas in foods of animal
origin have been conducted on products obtained at
the commercial level. Much higher percentages of
isolation were detected by Ibrahim and Mac Rae
(1991) in Australia, by Krovacek et al. (1992) in
Sweden, by Walker and Brooks (1993) in England, and
by Pin et al. (1994) in Spain, who respectively detected
100%, 60%, 50%, 57% and 40% positive samples. In
contrast, Knochel and Jeppesen (1990), Hudson and
Lacy (1991) and Rossi Júnior et al. (1996a), respectively analyzing products in Denmark, New Zealand
and Brazil, respectively, obtained results much closer
to those obtained in the present study, i.e. 25%, 21%
and 30% positive samples, even though these were
products commercially obtained. In a study on bovine
meat collected at a slaughterhouse, Rossi Júnior et al.
(1996b) found a 25% rate of contaminated samples, a
result closely similar to the 20% rate detected in the
present study. Table 1 also shows that a sample from
the environment of the slaughter room was positive,
demonstrating that this environment can act as a possible
source of contamination for the carcasses, organs and
viscera manipulated there.
With respect to the species detected, Table 1 shows that
Aeromonas caviae was present in the largest number of
samples compared to Aeromonas hydrophila and to
strains considered atypical. Several studies have
demonstrated the predominance of A. hydrophila over
A. caviae and A. sobria, (Majeed et al., 1989; Knochel
and Jeppesen, 1990; Gobat and Jemmi, 1993; Rossi
Júnior et al., 1996a). In contrast, Fathi and Moustafa
(1991) detected a predominance of Aeromonas caviae
in different types of beef products.
The presence of Aeromonas hydrophila, although in
a small number of samples (09/3.3%), should be a
source of concern for public health services, especially
because of its isolation from samples of boned meat
ready for commercialization, given the risk this may
represent to different segments of the population.
Aeromonas hydrophila has been characterized as the
species presenting the greatest pathogenic potential
(Cahill, 1990) and the one most frequently incriminated
in human infections (Ellison and Mostow, 1984;
Wadström and Ljung, 1991; Ko and Chuang, 1995).
Although Aeromonas hydrophila is the species
causing the greatest concern in terms of pathogenicity,
we should not overlook the presence of Aeromonas
caviae in 59 (21.8%) of the samples studied since this
microorganisms may also produce virulence factors,
though to a lesser extent, as reported by Cahill (1990),
Wadström and Ljung (1991) and Havelaar et al. (1992).
Aeromonas isolates considered to be atypical were
present in 13.0% of the samples studied (Table 1).
Hudson and Lacy (1991), Ibrahim and Mac Rae
(1991) and Pin et al. (1994) detected such strains in
meat from different types of butcher shops, as well as
in cow’s milk and in cheese.
Table 2 presents the data referring to the populations
of Aeromonas spp detected in the different types of
samples. Among boned meat samples, only one could
be counted, presenting a population of 2.0 x 10 CFU/g.
This number was much lower than that obtained by
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Rossi Júnior OD et al.
RPCV (2006) 101 (557-558) 125-129
Table 2 - Maximum and minimum populations and averages arithmetic’s of Aeromonas spp, in each type of samples collected at
different locations throughout the beef slaughtering process line
Type of samples
Positive samples
in the direct
inoculation for
quantification
Population of Aeromonas spp
Mínimum
Máximum
Average
0,2x10**
3,0x10
1,1X10
09(30,0)
0,2x10**
1,5x10
02(6,7)
0,2x10**
3,0x102
1,5X102
4,8x10
1,4x10
Dry hide surfaces – animals upon arrival
00(0,0)*
Surface of forequarter hide– after aspersion bath
07(23,3)
Surface of hindquarter hide–after aspersion bath
Surface of muscle tissue forequarter
Surface of muscle tissue hindquarter
00(0,0)
Deboned meat – commercial cuts
01(3,3)
Surface of knives
00(0,0)
Slaughter room area
01(3,3)
Intestinal content
07(23,3)
TOTAL
27(10,0)
2
3,1X10
2,0x10***
1,0x10***
* Percentage in relation to the total number of samples analyzed in each type.
** Colony forming units/cm2.
*** Colony forming units/gram.
Knochel and Jeppesen (1990) who found populations
higher than 105 CFU/g in beef, pork and fowl. Fathi
and Moustafa (1991) and Gobat and Jemmi (1993)
respectively detected populations of the order of 2.1 x 108
and 3.0 x 104 CFU/g in meat products and concluded
that these elevated populations were due to the lack of
hygienic-sanitary care in the preparation and commercialization of the products. It is important to point out
that the meat analyzed in the present study was collected at its source of production when it had not been
submitted to the frequently adverse situations of conservation that occur both during commercialization
and at the domestic level. The authors cited above are
unanimous in stating that Aeromonas can very well
develop during storage under refrigeration regardless
of faults in this process and point out that many strains
are psychrophilic.
The Aeromonas population detected in the intestinal
content, although relatively reduced, with a maximum
value of 1.4 x 10 CFU/g, was sufficient to permit its
identification and count from direct seeding, whereas
this was not possible in a study conducted by Gray and
Stickler (1989) who, working with feces of different
animal species, detected positive samples only after
enrichment.
The lack of information about the population of
bacteria of the genus Aeromonas in the remaining
types of samples analyzed in the present study impairs
a comparative analysis aiming at the establishment of
the significance and real magnitude of this population.
However, the data obtained should be considered
worrisome since the populations detected were sufficient to permit isolation and count by direct seeding, a
fact that was not possible in several other studies
(Figura and Marri, 1985; Hudson and Lacy, 1991;
Krovacek et al., 1992), and also because bacteria of the
128
genus Aeromonas can reach the meat during the various phases of the slaughtering process through the
outer surface of the animal’s body.
On the basis of the present results, we may infer that,
regardless of the hygienic-sanitary level of a slaughterhouse-meat processing plant, bovine meat can be contaminated with bacteria of the genus Aeromonas as
early as at the time when it is obtained.
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