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Aerobic bacterial flora of the respiratory
tract of healthy sheep slaughtered in Dessie
municipal abattoir, northeastern Ethiopia
N. YIMER1 AND B. ASSEGED2*
1
2
Gondar University, Faculty of Veterinary Science. PO Box 196, Gondar, ETHIOPIA
Addis Ababa University, Faculty of Veterinary Medicine. PO Box 34, Debre Zeit, ETHIOPIA
* Corresponding author: E-mail : assegedbogale@yahoo.com
SUMMARY
RÉSUMÉ
The aerobic bacterial flora of the respiratory tract were investigated using
samples collected from nasal cavity, tonsil, trachea and lung of 48 healthy
sheep slaughtered at Dessie Municipal Abattoir, Northeastern Ethiopia.
From a total of 192 specimens (48 from each anatomical sites), 160 (83.3%)
contained bacteria; animal infection rate was 100%. Tissue infection rates
on the other hand were 97.9%, 93.8%, 79.2% and 62.5%, respectively for
the nasal cavity, tonsil, trachea, and lung, indicating a general decrease in
the carrier state down the respiratory passageways. E. coli (14.2%) was the
predominant species, followed by Coagulase negative Staphylococcus
(10.7%), and Corynebacterium pseudotuberculosis and Bacillus species
(9.9% each); Citrobacter (2.6%) and Klebsiella (1.3%) were among the
least encountered bacterial genera. The majority of the bacterial species
inhabit all the anatomical sites; exceptions were E. coli, Enterobacter, and
Klebsiella spp, which were absent respectively from tonsil, lung, and trachea
and tonsil. Summing-up, Gram’s positive bacteria predominated over
Gram’s negative ones (62.2% vs. 37.8%) although both groups showed a
marked variation during the study period. The significance of this variation
in the pathogenic role of these commensals and its relation to extremes of
weather and other poor managerial inputs is an area of future research.
Flore bactérienne aérobie isolée des voies respiratoires de moutons
sains abattus à l’abattoii r municipal de Dessie, nord est de l’Ethiopie
Keywords: Abattoir, Aerobic bacteria, Dessie, Respiratory
tract, Sheep.
La flore bactérienne aerobique de la voie respiratoire a été étudiée en utilisant
des échantillons recueillis de la cavité nasale, les amygdales, la trachée et les
poumons de 48 moutons sains abattus à l’abattoir municipal de Dessie, au
Nord Est de l’Ethiopie. Sur un total de 192 échantillons (48 échantillons de
chaque endroit anatomique indiqué ci-dessus) 160 soit 83% contenaient des
bactéries. Le taux d’infection animal était de 100%. Le taux d’infection des
endroits anatomiques étaient 97.7%, 93.8%, 79.2%, et 62.5% respectivement
pour la cavité nasale, les amygdales, la trachée et les poumons. Ceci montre une
décroissance générale de l’infection au long des voies respiratoires de l’extérieur
vers l’intérieur. Eschericia coli (14.2%) était l’espèce dominante suivie par
le Staphylococcus spp. (10,7%). Corynebacterium pseudotuberculosis et
Bacillus spp ont été isolés dans 9.9% des cas, chacune. Citrobacter (2.6%)
et Klebsiella (1.3%) étaient parmi les moins présents. La majorité des bactéries
ont été isolées de tous les quatre endroits anatomiques mentionnés ci-dessus.
Seuls Eschericia coli, Enterobacter et Klebsiella spp étaient absents respectivement, des amygdales, des poumons et de la trachée. En général, il y avait
une prédominance de bactérie Gram positif (62.2%) sur le Gram négatif
(37.8%) bien que les deux groupes montrent une variation marquée pendant
la période d’étude. L’importance de cette variation dans le rôle pathogénique
des ces bactéries et sa relation aux extrêmes climatiques et aux mauvaises gestions
des moyens de production sera un domaine de recherche dans le futur.
Mots-clés : Abattoir, Bactérie aerobique, voie respiratoire,
Moutons, Dessie.
Introduction
Owing to their remarkable ability to adapt to diverse environmental conditions, sheep play an important role in traditional
smallholder farming systems of Ethiopia. The country’s holding
is currently estimated at 24 million [13]; and taking into
account the off take and growth rate, it is estimated that up
to 7000 tons of mutton can be put into export market annually
[16]. However, the country is supplying considerably less,
mainly due to the widespread zoonotic and epidemic diseases.
THOMSON [33] stated that diseases affecting the respiratory
system are generally the most important in all species of
domestic animals. Accordingly, though the types and numbers
may vary greatly with age, geographic location, nutrition and
climate, a wide variety of bacteria are found in the respiratory
tract. This implies that the respiratory tract is more accessible
to injurious agents although major airways and lung parenchyma
Revue Méd. Vét., 2007, 158, 10, 473-478
neutralize or remove the infectious agents that are deposited,
so that the deeper structures are less often attacked [9].
Nonetheless, the effects of infection in the deeper structures
are more severe and more ominous than in the upper respiratory tract [14].
Respiratory diseases of various etiologies have been described in different domestic animals. However, the problem
is more common in sheep due to the fact that the ratio of the
alveolar surface to metabolic weight is very low in sheep
compared to other species [11]. As a result, many specific
primary pathogens have been implicated in sheep pneumonia
[36]. However, it is becoming increasingly difficult to make
an etiological diagnosis because, although a single agent may
be a primary invader, when the local resistance of respiratory
mucosa is lowered, bacteria growing in the nose and throat
extend downwards, usually producing multiple bacterial
infections [17]. Besides, most of the infectious agents causing
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respiratory disease are ubiquitous in nature and are normal
inhabitants of the nasopharynx. This often creates difficulty
in interpreting microbiological findings during an outbreak
of respiratory diseases [23].
Several studies conducted in Ethiopia mainly focus on the
bacterial flora of pneumonic lungs of sheep, cattle and camel
[1, 5, 26, 29, 31], and there are no published reports regarding
the microflora of normal respiratory passageways. This
information is however central to the understanding of the
causes of respiratory diseases. This study was therefore designed
to isolate and characterize aerobic bacteria from different
anatomical sites of the respiratory passageways of apparently
healthy sheep.
YIMER (N) AND ASSEGED (B)
BACTERIOLOGIC EXAMINATION
After 24 h of incubation, the cultured samples were thoroughly
agitated to aid mixing. Then, a loopful of the broth culture
was taken and streaked over an identified petri-plate containing
blood agar base supplemented with 7% sheep blood [22].
The plates were labeled and incubated aerobically at 37 ºC
for 24-48 h [2].
The study was conducted from November 2004 to April
2005, in Dessie Township, 401 km Northeast of Addis
Ababa. The mean annual rainfall and the mean day-night air
temperature ranges are respectively 750-1000 mm3 and
11.7-23.9 ºC. The relative humidity varies from 23.9%-79%.
After taking note of cultural characteristics, positive cultures
were subjected to Gram’s staining to study staining reaction
and cellular morphology under light microscope, at 100X
magnification. Mixed colonies and Gram-negative bacteria
were sub-cultured on both blood and McConkey agar plates
[22] for further analysis. Pure cultures of single colony type,
from both blood and McConkey agars, were transferred onto
nutrient agar-slants for a series of primary tests: catalase
(Hydrogen peroxide, Fisher Chemical, UK), oxidase (TM-pphenylenediamine dihydrocholoide, Merck Co., Germany)
and fermentative/oxidative (OF Basal Medium, Titan
Biotech Ltd, India); and secondary tests: urease (urea and
urease, Labort Co., India), coagulase (rabbit plasma), indole
(Peptone water, Merck Co., Germany) and H2S (Triple
Sugar Iron Agar, Merck co., Germany), following standard
procedures [9, 22].
STUDY ANIMALS
DATA ANALYSIS
The study was carried out on 48 local highland fat-tailed
sheep, randomly selected at Dessie Municipal Abattoir. The
animals were raised in a communal pasture under traditional
management practices. Although records were lacking regarding
age and previous health status, all the sheep were adult males
and were clinically normal during ante-mortem examination.
Descriptive statistics were used to summarize the data
generated from examining each of the study animals and different anatomical sites. Accordingly, the relative abundance
of each species/genera was expressed as a percentage in
comparison to the total number of isolates. Similarly, the
relative proportion of infections at each anatomical site was
expressed as a percentage.
Materials and Methods
STUDY AREA
SAMPLE COLLECTION
The nasal samples were collected, during ante-mortem
inspection, by inserting sterile cotton-tipped applicator sticks
into the nasal passageways after proper cleaning and disinfection of the external nares. Following the slaughter of the
identified animal, the trachea was grasped with tissue forceps
and partially opened by sterile scalpel blade. Then, a long
cotton-tipped swab was inserted into the opened tracheal
tube, ensuring effective contact with the mucosa. The swabs
were put in separate sterile test tubes into which 3 ml
Tryptone soya broth was added [9], labeled and kept in a
cool box, and transported to the nearby Kombolcha Regional
Veterinary Laboratory for immediate incubation at 37 °C for
24 hours [22].
Before collecting tonsil and lung samples, the external surfaces were disinfected with 70% alcohol [9] to minimize surface
contamination. Using sterile scissors and thumb forceps, pieces
of the lung and the corresponding tonsil were collected separately into sterile screw-capped universal bottles. Then, in a
closed room with sprit burner, the samples were flamed and
about 10g of each was transferred into another universal bottle
containing 3 ml tryptone soya broth. After labeling, these were
transported in an icebox to Kombolcha Regional Veterinary
Laboratory and incubated aerobically at 37 °C for 24 hours.
Results
Out of 192 specimens collected from nasal cavity, trachea,
tonsil and lung (48 from each site), 160 (83.3%) harbored
bacteria; animal infection rate was 100% (Table I). In general,
233 different bacteria were isolated from 160 infected specimens,
accounting for 1.46 bacteria per infected sample; a corresponding
bacterial burden per animal was 4 (194/48). The relative proportion of bacterial species identified is indicated on Figure 1.
The predominant species among the isolates were E. coli
(14.2%), followed by CNS (10.7%), and Corynebacterium
pseudotuberculosis and Bacillus species (9.9% each). On the
other hand, Klebsiella (1.3%) and Citrobacter (2.6%) were
among the least encountered bacterial genera.
The majority of the isolates colonize all the anatomical
sites investigated; exceptions were E. coli, Enterobacter and
Klebsiella species, which were absent from tonsil, lung, and
trachea and tonsil respectively (Fig. 2). However, a general
decrease in the isolation rate was observed as one goes down
the respiratory tract; respective sites with the highest and
lowest infection rates being the nasal cavity (47/48) and the
lung (30/48) (Table I). In a nutshell, G+ve bacteria are the
predominant species inhabiting the respiratory tract of apparently
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AEROBIC BACTERIAL FLORA OF THE RESPIRATORY TRACT OF HEALTHY SHEEP, NORTHEASTERN ETHIOPIA
healthy sheep in this environment although the proportion of
G-ve bacteria rose dramatically during the first half of the
study period (Fig. 3).
Discussion
This study has shown that a wide variety of bacteria colonize
the respiratory tract of apparently healthy sheep. Several
workers [4, 7, 24] previously isolated similar bacteria from
pneumonic lungs of sheep, while others [3, 19, 20, 35] isolated
them from pneumonic caprine lungs. In addition, SHEMSEDIN
[26] and SHIGIDI [28] isolated similar species from pneumonic lungs of camels. The invariable isolation of these
organisms from the pneumonic lungs of various animal species
indicates their potential role in different respiratory syndromes.
Mannheimia hemolytica was isolated in higher proportion
from tonsil although lung infection rate was considerable
(Fig. 2). Similarly high tonsil carrier state has been reported
previously [29]. M. hemolytica is normal inhabitant of upper
respiratory tract although it might cause secondary bronchopneumonia after primary initiating agent has suppressed
the host defense mechanism [6, 9, 30]. In line with this,
MOHAMMED [19] reported higher incidence rates from
pneumonic lungs. Similarly, Pasteurella multocida frequently
inhabited tonsil and nasal cavity (Fig. 2). This is in agreement
with previous reports [3, 19], indicating that the organism
lives as a commensal in the upper respiratory tract, invading
the lung under conditions of stress [12]. In agreement with
previous reports [5, 23, 29], both in terms of infection intensity
and pathogenicity, it seems that M. hemolytica assumes greater
prominence in ovine respiratory syndromes in this environment.
FIGURE 1: Relative proportion of different aerobic bacteria isolated from
respiratory tract of healthy sheep at slaughter.
FIGURE 2: Proportions of bacterial isolates in relation to anatomical
location.
FIGURE 3: Dynamics of G+ve and G-ve bacteria during the study period.
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YIMER (N) AND ASSEGED (B)
ID
Anatomical sites
Nasal
Cavity Tonsil Trachea
ID
Lung
Isolates
per
animal
Anatomical sites
Nasal
Cavity Tonsil Trachea
Lung
Isolates
per
animal
1
2
-
1
-
3
25
2
1
1
1
4
2
1
1
-
-
2
26
1
2
1
-
3
3
2
1
-
-
3
27
-
2
2
2
6
4
2
1
1
-
3
28
2
1
1
1
4
5
1
1
2
1
3
29
4
1
1
1
4
6
1
2
1
1
4
30
3
2
2
1
8
7
1
1
-
2
2
31
1
1
2
-
4
8
2
2
1
1
6
32
2
3
2
1
5
9
1
1
2
1
4
33
2
1
2
1
6
10
2
1
2
-
4
34
2
2
1
2
7
11
3
1
2
1
5
35
2
2
1
2
5
12
1
2
2
-
4
36
1
2
1
2
5
13
3
2
1
-
5
37
3
1
1
-
5
14
2
2
1
-
4
38
1
2
-
1
3
15
1
1
2
-
4
39
1
1
-
2
4
16
2
-
1
-
2
40
3
2
1
1
6
17
1
1
1
-
3
41
2
1
-
2
4
18
2
1
1
-
4
42
2
-
-
2
3
19
1
1
1
1
3
43
1
1
2
2
5
20
1
1
1
1
3
44
2
1
-
-
3
21
2
1
-
-
3
45
2
1
2
1
4
22
1
2
1
1
3
46
1
1
1
-
3
23
1
1
1
1
4
47
1
2
1
1
4
24
2
1
1
2
5
48
1
1
-
1
3
Total
80
62
51
40
1994
TABLE 1: A summary of study animals and anatomical sites examined alongside the number of isolates per infected tissues and per animal.
The finding that E. coli was the predominant species
conforms well to the previous study involving ovine lungs
[19]. However, TESFAYE [32] failed to isolate E. coli from
trachea and lung of apparently healthy goats. The discrepancy
could be attributed to the difference in the feeding habits of
the two species: sheep usually prefer to graze down to the
ground [15] and hence have a high chance of ingesting bacteria
from the soil. On the other hand, the absence of E. coli in the
tonsil (Fig. 2) reveals its transient nature, not playing much
of a pathogenic role [12]. However, it has been suggested
that E. coli, which is usually harmless in its normal habitat,
could cause pulmonary and urogenital infections [21].
CNS was the second dominant bacteria (Fig. 1), mainly
inhabiting the nasal cavity (12.5%) and trachea (11.8%).
MEGRA et al. [18] and TESFAYE [32] similarly isolated
CNS mainly from nasal cavity and trachea of goats. CNS
often involves in the pharyngeal and lung abscesses, and
suppuration of other parts of the respiratory tract when
defense mechanism of the host is compromised [25, 27].
C. pseudotuberculosis was isolated from all anatomical
sites (Fig. 2) with relative abundance in the tonsil and lung.
This finding is in agreement with previous reports [3, 19]
although others [18, 32] isolated the organism only from
nasal cavity and lung. It has been established that C. pseudotuberculosis is inhaled into respiratory tract from skin and
mucous membranes [9]. Similarly, Bacillus spp was isolated
mainly from tonsil and trachea (Fig. 2). MOHAMMED [19]
previously isolated Bacillus spp from trachea and lung of
sheep and goats although SHEMSEDIN [26] isolated only
from camel’s lung. On the other hand, AJUWAPE and
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AREGBESOLA [2] failed to isolate the agent from the nasal
swab of normal rabbits.
In contrast to previous report [18, 32], Actinomyces pyogenes
was isolated mainly from the lung (Fig. 2). It has been stated
that A. pyogenes is a commensal of the nasopharyngeal
mucosa and causes disseminated purulent infections when
the animal is stressed [30]. It may also reside as a commensal
on the respiratory linings with a threat of causing pulmonary
abscess and bronchopneumonia [34]. Several workers [3, 7,
19] have similarly isolated A. pyogenes from nasal cavity
and lung.
Streptococcus zooepidemicus was one of the most frequently encountered species (Fig. 2), with the highest incidence
in the tonsil (12.9%). BUXTON and FRASER [8] indicated
that Streptococcus is widely distributed in nature and lives as
a commensal in the respiratory tract of many species of
domestic animals, although potentially pathogenic species
do exist [10].
Nasal cavity and trachea were the commonest sites for
Enterococcus faecalis (Fig. 2), although the bacterium has a
chance of reaching there either by inhalation or through
hematogenous route. The bacterium lives in the intestinal
tract (natural habitat) and might cause opportunistic infections such as endocarditis in sheep [22]. On the other hand,
Staphylococcus aureus was isolated mainly from the nasal
cavity (Fig. 2) although the incidence (6.3%) was much
lower compared to previous 100% isolation rate in rabbit [2].
This variation could be attributed to a feeding habit (rabbits
are coprophagous) [15] but the extensive management under
which the sheep were kept might have also contributed to the
comparatively lower nasal involvement. However, the lung
isolation rate (4.2%) was in agreement with previous study
in goats [3] although much higher rates have been reported
from pneumonic lungs of sheep [7, 19] and goats [19, 35].
According to ROBBINS et al [25], S. aureus is the main
inhabitant of the upper respiratory mucosa, playing a pathogenic
role in immunocompromised hosts. It also has zoonotic
implications, with opportunities for reciprocal transmission
between man and domestic animals when natural barriers are
compromised [2].
Micrococcus, whose ubiquity is primarily due to contamination from skin [9], was isolated from all anatomical sites:
trachea and lung were more frequently involved (Fig. 2).
Similarly, Pseudomonas aeruginosa was more prevalent in
the trachea (Fig. 2). Previous workers isolated the agent from
nasal cavity of apparently healthy rabbit [2] and from pneumonic lung of sheep [20]. P. aeruginosa can be found on the
skin, mucous membranes and in the feces, causing pneumonia
and lung abscess in sheep and goats [22].
Enterobacter, Citrobacter and Klebsiella, predominantly
inhabited the nasal cavity and tonsil (Fig. 2). Enterobacter
has been isolated from respiratory tract of camel [26], whereas
Klebesiella, a common saprophyte in the soil and respiratory
tract of various animals, was reported from nasal cavity of
apparently healthy rabbits [2]. The isolation of these organisms (including E. coli) in the absence of clinical enteritis is
note worthy.
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477
Summing up, although the level of G+ve bacteria was
generally high (Fig. 3) the proportion of G-ve bacteria rose
during the first half of the study period (November-January).
This period coincides with low environmental temperatures,
representing a recognizable stressful condition. Considering
these extremes of weather and other poor managerial inputs,
the pathogenic role of these apparently commensal organisms could be enormous. We therefore recommend a detailed
study to look into the economic impact of these organisms.
Acknowledgements
The authors would like to thank the officials of
Kombolcha Regional Veterinary Laboratory and Dessie
Municipal Abattoir for provision of materials and other technical support. The technical guidance and material support of
Dr. Araya Mengistu and Dr. Ademe Zerihun is well recognized.
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