https://doi.org/10.52973/rcfcv-e34389
Received: 12/02/2024 Accepted: 02/04/2024 Published: 14/07/2024
1 of 8
Revista Científica, FCV-LUZ / Vol. XXXIV, rcfcv-e34389
ABSTRACT
Food of animal origin such as milk and meat have a high nutritional
value and form an important part of the human and animal diet,
but are dicult to produce and are highly perishable. Additionally
signicant socio–economic loss will result if production and/or
storage conditions are neglected, whether through loss of the food
or illnesses caused by consumption and treatment. It was in this
context that we carried out this study, to assess the hygienic quality
of cows milk and meat produced and consumed in a border region
of Algeria. A total of 130 samples were taken from animal foodstuffs
(raw cows milk, sheep carcasses, chicken and turkey meat) at farm,
abattoir and butchery levels. Mesophilic aerobic ora, total coliforms,
thermotolerant coliforms and Escherichia coli were enumerated, and
the sensitivity of the E. coli to certain antibiotics most commonly
used in human and veterinary medicine was assessed. High levels of
contamination and bacterial loads ranging from 5.36×10
2
CFU·mL
–1
for
milk, to 1.56×10
5
CFU·cm
–2
for sheep meat, some of this foodstuffs are
acceptable but represent a food hazard, and others are not acceptable
according to regulations. A high percentage of multiresistant strains
and worrying resistance rates were detected, and if the necessary
measures are not taken as a matter of urgency in the context of
“One Health”, the situation is likely to worsen and human and animal
health will be affected.
Key words: Food of animal origin; microbiological quality; E. coli;
antibiotic resistance; Algeria
RESUMEN
Los alimentos de origen animal como la leche y la carne tienen un alto
valor nutricional y forman una parte importante de la dieta humana y
animal, pero son difíciles de producir y muy perecederos. Además,
si se descuidan las condiciones de producción y/o almacenamiento,
el resultado será una pérdida socioeconómica signicativa, ya sea
por la pérdida de alimentos o por enfermedades causadas por el
consumo y el tratamiento. Fue en este contexto que llevamos a cabo
este estudio, para evaluar la calidad higiénica de la leche y la carne
de vaca producidas y consumidas en una región fronteriza de Argelia.
Se tomaron un total de 130 muestras de alimentos de origen animal
(leche cruda de vaca, canales de oveja, carne de pollo y pavo) a nivel
de granja, matadero y carnicería. Se enumeraron la ora aeróbica
mesóla, los coliformes totales, los coliformes termotolerantes y
Escherichia coli, y se evaluó la sensibilidad de las E. coli a ciertos
antibióticos más comúnmente utilizados en medicina humana y
veterinaria. Altos niveles de contaminación y cargas bacterianas
que van desde 5,36×10
2
CFU·mL
–1
para la leche, hasta 1,56×10
5
CF·cm
–2
para la carne de ovino, algunos de nuestros alimentos son aceptables
pero representan un peligro alimentario, y otros no son aceptables
según las regulaciones. Se detectó un alto porcentaje de cepas
multirresistentes y tasas de resistencia preocupantes, y si no se
toman urgentemente las medidas necesarias en el contexto de “Una
sola salud”, es probable que la situación empeore y la salud humana
y animal se vea afectada.
Palabras clave: Alimentos de origen animal; calidad microbiológica;
E. coli; resistencia antibiótica; Argelia
Hygienic quality of food from animal origin and antibiotic resistance of
Escherichia coli in a border region of Algeria
Calidad higiénica de los alimentos de origen animal y resistencia a los
antibióticos de Escherichia coli en una región fronteriza de Argelia
Soane Tamendjari
1,2
* , Khelaf Saidani
3
, Lina Chaib
1
, Hebib Aggad
4
, Zoubir Bouzebda
1,2
, Farida Afri Bouzebda
1,2
1
Mohamed Cherif Messaadia University, Institute of Agricultural and Veterinary Sciences, Department of Veterinary Sciences. Souk Ahras, Algeria.
2
Mohamed–Cherif Messaadia University, Institute of Agricultural and Veterinary Sciences,
Laboratory of Animal Productions, Biotechnologies and Health (PABIOS). Souk Ahras, Algeria.
3
BLIDA1 University, Institute of Veterinary Science. Blida, Algeria.
4
Ibn Khaldoun University, Institute of Veterinary Science, Laboratory of Hygiene and Animal Pathology. Tiaret, Algeria.
*Corresponding Author: s.tamandjari@univ–soukahras.dz | soanetam06@gmail.com
Hygienic quality of food from animal origin and antibiotic resistance / Tamendjari et al. ____________________________________________
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INTRODUCTION
Foodstuffs of animal origin are highly nutrient dense and have
excellent taste qualities. However, they are subject to contamination
and inevitable bacterial attack as they contain elements necessary
for their development [1]. Their presence in a food has three
consequences : enhancement, as in the case of fermented foods,
or degradation, as in the case of contamination by bacteria with high
enzymatic power such as mesophilic aerobic ora, psychrotrophs
and Escherichia coli, or containing a health hazard without any
organoleptic modification of the food, such as Mycobacterium
tuberculosis, Brucella (causative of brucellosis) or certain species
of virulent E. coli. This is why inspection and microbiological analysis
of foodstuffs is so important, from production to consumption, or
from the farm to the table [2].
The initial number of bacteria and their species determine the shelf
life of a foodstuff. In order to guarantee a healthy, safe, nutritious and
sucient food supply this concept is enshrined as one of the four
pillars of food safety [3]. Consumption of food contaminated with
undesirable bacteria can lead to various types of food poisoning,
ranging in severity from a simple disturbance of the intestinal
microbiota in the form of diarrhea to the infection and invasion of
the entire organism. It is estimated that one person in ten falls ill after
consuming contaminated food, causing 420,000 deaths every year,
along with economic losses [4]. In either events mentioned above,
antibiotics are used to eliminate the undesirable bacteria which may
then be replaced by the normal ora. Concerningly, this approach can
fail to work, especially in regions without access to advanced medical
care, due to the increasing emergence of antibiotic–resistant strains
of bacteria causing foodborne illness.
The United Nations is attempting to remedy this situation by
proposing a “One Health” approach, and it is in this context that this
study was carried out, to determine the hygienic quality of raw milk
and meat of different animal origin consumed in a border region of
Algeria, namely Souk Ahras, and to assess the antibiotic resistance
of E. coli isolated from food of animal origin [5].
MATERIALS AND METHODS
Area and period of study
This study took place at the Institute of Agricultural Sciences and
Veterinary Sciences, laboratory of Animal Productions, Biotechnologies
and Health (PABIOS), Mohamed–Cherif Messaadia University – Souk
Ahras, Algeria, from March 2019 to September 2020, and from
September 2021 to June 2022 (due to COVID19).
Sample collection
A total of 130 samples were taken from the Souk Ahras region,
including 40 samples of raw cows milk (Bos taurus), 30 samples of
sheep (Ovis aries) meat, 30 samples of chicken (Gallus gallus domesticus)
meat and 30 samples of turkey (Meleagris gallopavo domesticus) meat.
Samples of raw cows milk were taken after udder cleaning and
disinfection on three farms, and the milk found apparently t for
consumption, i.e. no change in organoleptic characteristics was
observed. Ovine carcasses were sampled using a sterile scalpel blade
[6] just after stamping, at the Souk Ahras municipal slaughterhouse.
Samples of chicken and turkey meat were taken from various butchers
shops in the region, to reect the same conditions of sale to the
consumer. Each sample was placed in a sterile bottle, marked with
an identier, placed in a cooler with ice packs (Abbott–ICECATCH)
and sent to the laboratory.
Sample processing
All samples were processed in the laboratory within a few hours
of collection: Milk samples were diluted directly with peptone water
to obtain the various decimal solutions. For sheep meat, a volume of
100mL of sterilized peptone water was added to each sample to obtain
a 10
-1
stock solution, then different decimal dilutions were prepared.
For chicken and turkey meat, the sample in its bottle was weighed
(Pionner
tm
, Plus Precision Ohaus®, USA), the weight of the sample is
deducted, and a volume (peptone water) of nine times the weight of
the sample was added to obtain a 10
-1
stock solution, in order to avoid
any manipulation of the sample and any modication of the existing
ora. Decimal solutions were then prepared [7].
Enumeration of mesophilic aerobic ora, coliforms, thermotolerant
coliforms and E. coli
One (1) mL of each decimal dilution was inoculated on to PCA (Plate
Count Agar) culture medium (Institut Pasteur Algérie) and incubated
(UNB 400, Memmert, Germany) at 30°C for 72 hours (h) for mesophilic
aerobic ora (MAF) enumeration. All colonies were counted [8].
One (1) mL of each dilution was placed on a Petri dish before pouring
a rst layer of Violet Red Bile Lactose Agar medium (VRBL) (Difco) and
mixing with a second layer added after gelling, Petri dish were then
incubated at 30°C for 24 to 48 h for coliforms enumeration and at 44°C for
24 to 48 h for thermotolerant coliforms enumeration. All pink–red colonies
with a diameter greater than or equal to 0.5 mm were counted [8].
Enumeration was performed using the following formula N = ƩC /
V × 1.1 × d, on plates with 10 to 300 colonies [9].
N (CFU): number of microorganisms present in the sample.
ƩC: sum of colonies counted from the two dilutions retained.
V: volume inoculated (1 mL).
d: the dilution rate of the rst dilution retained for the counts.
For raw cows milk, dilutions 10
-1
and 10
-2
were retained for the
enumeration of MAF, coliforms and thermotolerant coliforms.
For chicken and turkey meat, dilutions 10
-2
and 10
-3
were retained
for the counts of MAF, coliforms and thermotolerant coliforms.
Dilutions of 10
-3
and 10
-4
were used for the enumeration of MAF in
ovine meat, and dilutions of 10
-2
and 10
-3
were used for the enumeration
of coliforms and thermotolerant coliforms.
For E. coli identication, colonies of thermotolerant coliforms
were isolated and puried for identication on the API E20 gallery
(BioMérieux, France), then their counts were deduced.
Evaluation of antibiotic resistance
Antibiotic resistance of identied E. coli strains was assessed on
Muller–Hinton agar according to CLSI performance standards [5],
after reviving the preserved strains.
The antibiotic discs (Liofilchem, Roeseto, Italy) used were:
Penicillin (P) (10); Ampicillin (AMP) (10); Amoxicillin/clavulanic acid
(AMC) (20/10); Cefoxitin (FOX) (30); Gentamycin (CN) (10) ; Kanamycin
TABLE I
Contamination rates of various foods of animal origin
MAF
Total
coliforms
Thermotolerant
coliforms
Escherichia coli
Raw cow milk 40(100%)
a
20(50%)*
b
8(20%)*
c
7(17.5%)*
c
Ovine carcass 30(100%)
a
30(100%)**
a
27(90%)**
ab
26(86.66%)**
b
Chicken meat 30(100%)
a
14(46.66%)*
bcd
10(33.33%)*
cd
9(30%)*
d
Turkey meat 30(100%)
a
13(43.33%)*
b
9(30%)*
b
9(30%)*
b
*: signicant dierence (P<0.05) read vertically.
a,b,c,d
: signicant dierence (P<0.05)
read horizontally
FIGURE 1. Contamination rates of various food of animal origin
TABLE II
Average loads of MAF, Total coliforms, thermotolerant coliforms and E. coli isolated from various foods of animal origin
MAF
(mean ± sd)
Total coliforms
(mean ± sd)
Thermotolerant
coliforms (mean ± sd)
Escherichia coli
(mean ± sd)
Raw cow milk
(CFU·mL
–1
)
5.36×10
2
± 2.62×10
2
*
Min: 2.10
2
Max: 1.26.10
3
5.16.10
2
± 2.20×10
2
*
Min: 2.27×10
2
Max: 1.03×10
3
5.69×10
2
± 1.57×10
2
*
Min: 3.00×10
2
Max: 8.64×10
2
5.82×10
2
± 1.65×10
2
*
Min: 3.00×10
2
Max: 8.64×10
2
Ovine carcass
(CFU·cm
–2
)
8.34×10
4
± 3.48×10
4
****
Min: 2.9×10
4
Max: 1.56×10
5
6.2×10
3
± 2.65×10
3
****
Min: 2.64.10
3
Max: 1.11×10
4
5.08×10
3
± 1.98×10
3
***
Min: 2.36×10
3
Max: 9.36×10
3
5.17×10
3
± 1.95×10
3
*
Min: 2.36×10
3
Max: 9.36×10
3
Chiken meat
(CFU·g
–1
)
8.6×10
3
± 3.52×10
3
***
Min: 3.45×10
3
Max: 1.65×10
4
8.64×10
3
± 1.73×10
3
***
Min: 5.09×10
3
Max: 1.09×10
4
6.5×10
3
± 2.04×10
3
***
Min: 3.09×10
3
Max: 9.82×10
3
6.13×10
3
± 1.77×10
3
***
Min: 3.09×10
3
Max: 8.45×10
3
Turkey meat
(CFU·g
–1
)
5.25×10
3
± 2.7×10
3
**
Min: 3.18×10
3
Max: 1.35×10
4
3.53×10
3
± 6.36×10
2
**
Min: 2.64×10
3
Max: 4.73×10
3
3.47×10
3
± 6.47×10
2
**
Min: 2.55×10
3
Max: 4.45×10
3
3.47×10
3
± 6.47×10
2
**
Min: 2.55×10
3
Max: 4.45×10
3
sd: standard deviation. *: signicant dierence (P<0.05) read vertically, except for chicken and turkey meat, read vertically and horizontally (CFU·g
-1
, both)
_____________________________________________________________________________Revista Cientifica, FCV-LUZ / Vol. XXXIV, rcfcv-e34389
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(K) (30) ; Ooxacin (OFX) (5) ; Erythromycin (E) (30) ; Tetracycline (TE)
(30) ; Sulfonamide (SMZ) (50) ; Sulfonamides/Trimetoprim (SXT) (1.
25/23.75); Chloramphenicol (C) (30); Fosfomycin (FOS) (50).
Statistical processing of the results, i.e. comparison of means, analysis
of variance and degree of similarity of the E. coli strains identied, was
carried out using STATISTICA 7 software (Statsoft, France) [10].
RESULTS AND DISCUSSION
Prevalence of contamination and bacterial enumeration
The contamination rates of various foods of animal origin (TABLEI)
is shown in FIG.1.
The counts of MAF, total coliforms, thermotolerant coliforms and
E. coli identied in the various foods of animal origin are shown in
TABLE II with their maximum and minimum values.
In Algeria, similar contamination rates for milk were reported [11, 12]
but with higher bacterial loads for MAF and thermotolerant coliforms
[11, 13]. The average load of thermotolerant coliforms in this samples
is close to that reported by Aggad et al. [12] (2×10
2
CFU·mL
–1
), and
according to Algerian regulations regarding the microbiological criteria
applied to foodstuffs established in the Ocial Journal of the Republic
of Algeria Nº39 (Art. 6, Annex 1) these results are satisfactory [14].
Additionally, but the problem resides in the bacterial species known by
its opportunistic and pathogenic aspect that colonize the udder and
cause mammary gland infection at the slightest opportunity.
In some African countries, extremely high bacterial loads of MAF,
coliforms and thermotolerant coliforms in milk have been reported
[15, 16, 17] with average loads of E. coli reaching 2×10
6
CFU·mL
–1
(6.3Log
10
CFU·mL
–1
) in raw milk at farm level in Ethiopia [15].
Milk from a healthy animal may contain microorganisms, even if
sampled in good conditions. These are saprophytic germs of the udder
and galactophore ducts and can reach bacterial loads of 10
3
CFU·mL
–1
[8] to 10
5
CFU·mL
–1
[18].
It should be remembered that the initial number of bacteria in a food
product signicantly affects its freshness, add to this the numerous
manipulations and the time it takes to reach the processing industries [19],
which enhance a bacterial multiplication, and if the product is immediately
sold to public markets, a food poisoning is most likely to occur.
All sheep carcasses were contaminated with MAF and coliforms,
with average bacterial loads of 8.34×10
4
CFU.cm
–2
and 6.2×10
3
CFU·cm
–2
, respectively. The rate of contamination by thermotolerant
coliforms (5.08×10
3
CFU·cm
–2
) and E. coli (5.17×10
3
CFU·cm
–2
) was 90
and 86.66%, respectively.
Dis t. A gré gat io n
0,0 0,5 1,0 1,5 2,0
Ch5 - P/AMP/E/TE/SMZ/C/FOS
Ov14 - P/AMP/AMC/CN/K/E/TE/SMZ/SXT
Ov9 - P/AMP/AMC/CN/K/SMZ
Ov4 - P/AMP/AMC/FOX/OFX/SMZ
Ov17 - P/AMP/CN/K/OFX/E/TE/SMZ
Mi26 - P/AMP/CN/K/OFX/E/TE
T26 - P/AMP/E/TE/SMZ/SXT
T24 - P/AMP/AMC/OFX/E/TE/SMZ/C
T22 - P
T17 - P/AMP/OFX/SMZ
T11 - P/AMP/AMC/OFX/E/TE/SMZ
T9 - P/AMP/OFX/TE/SMZ
Ch30 - P/AMP/SMZ/SXT
Ch23 - P/AMP/C
Ch14 - P/AMP/OFX/E/TE/SMZ
Ov25 - P/AMP/AMC/FOX/TE/OFX/E/SMZ/SXT
Ch10 - P/AMP/AMC/OFX/E/TE/SMZ/SXT
Ov7 - P/AMP/AMC/E/TE/OFX/SMZ/SXT
Mi39 - P/AMP/AMC/OFX/SMZ/SXT
Ov30 - P/AMP/AMC/TE/OFX/SMZ/SXT
Ov24 - P/AMP/AMC/E
Ov28 - P/AMP/AMC
Ov22 - P/AMP/AMC/SMZ
Ov21 - P/AMP/AMC/SMZ
Ov16 - P/AMP/AMC/E/TE/SMZ
Ov12 - E/TE/SXM
Ov8 - TE
Ch7 -
Ov13 -
Mi37 -
Mi25 - SMZ
Ov5 - TE/SMZ
Ov15 - P/TE/SXM
Ch18 - P/AMP/AMC/OFX/TE/SMZ
Ov11 - P/AMP/AMC/OFX/TE/SMZ
Ov10 - P/AMP/TE
T15 - P/AMP
T5 - P/AMP
Ch15 - P/AMP
Ch6 - P/AMP
Ov26 - P/AMP
Ov23 - P/AMP
Ov6 - P/ A MP
Mi38 - P/AMP/E/TE
Ov2 - P/AMP/E/TE/SMZ
T2 - P/AMP/SMZ
Mi40 - P/AMP/ SMZ
Ov3 - P/AMP/TE/SMZ
Ov18 - P/AMP/AMC/TE/SMZ
Ov1 - P/AMP/AMC/TE/SMZ
Mi5 - P/AMP/AMC/TE/SMZ/SXT
FIGURE 2. Degree of similarity between Escherichia coli strains identied according
to their resistance proles to the antibiotics tested
Hygienic quality of food from animal origin and antibiotic resistance / Tamendjari et al. ____________________________________________
4 of 8
This results are close to those reported by Harhoura et al. [20] in
Algeria, and Jaja et al. (2018) [21] in South Africa, but lower bacterial
loads were reported by Djenidi (2016) [22], Nouichi et al. (2009) [23]
and El Hadef et al. [24], in Algeria.
Contamination of carcasses by MAF is inevitable, but contamination
by coliforms, thermotolerant coliforms and E. coli means contamination
by intestinal contents, which are the result of a lack of hygiene during
slaughtering, skinning, and evisceration. At the slaughterhouse, we
noticed the absence of specic clothing for personnel, a single knife
and a sharpening rie tool for all stages of primary processing, failure
to perform the forward motion principle, with sheep being worked on
the oor in dorsal recumbency, no clear separation between the clean
and soiled sectors, and a single slaughter room where all operations are
carried out, including the stamping and weighing of ovine carcasses.
For the tested white meats, there was no signicant difference between
the contamination rate of chicken and turkey meat, but the bacterial load
of chicken meat was higher than that of turkey meat (P<0.05).
Contamination rates higher than these results were reported in
Algeria [25, 26], Morocco [27] and Mexico [28]. This results are similar
to those reported in Italy [29], Sri Lanka [30], Thailand [31], and
Bangladesh [32] for frozen chicken meats, bearing in mind that cold
does not sanitize the food, hence the importance of refrigerating and
freezing a healthy food as soon as possible and without interruption
of cold throughout the storage period.
Higher MAF and E. coli bacterial loads were reported in western
Algeria [33], but lower bacterial loads are reported in eastern Algeria
[26]. This results are close to those reported in Turkey by Eyi and
Aslan [34], and in view of Algerian [14] and European [35] regulations,
these chicken and turkey meats are not acceptable given the high
bacterial load, to be specied that in Algerian regulations, only the
bacterial load of E. coli is mentioned [14].
The bacterial loads reported in this study indicate poor hygiene and/
or handling conditions, and it is dicult to identify where hygiene
conditions have failed, because the traceability and origin of these
meats is unknown, even if butchers have a health certicate, but the
absence of packaging and labels make identication impossible,
especially that many slaughtering is carried out clandestinely in order
to increase the prot margin.
Antibiotic resistance
The resistance frequencies of the E. coli identied towards the
antibiotics tested are shown in the TABLE III and the resistance
proles of the E. coli strains towards the antibiotics are shown in the
dendrogram in the FIG. 2 while studying the degree of approximation
of the E. coli strains identied.
TABLE III
Resistance frequencies of the Escherichia coli identied from dierent animal origin foodstu
Antibiotic family Antibiotics
Milk
(07 strains)
Ovin meat
(26 strains)
Chiken meat
(09 strains)
Turkey meat
(09 strains)
Total
(51 strains)
Beta–lactam
Penicilline
h
71.42 84.61 88.88 100 86.27
Ampicilline
h
71.42 80.76 88.88 88.88 82.35
Amoxycilline/ Clavulanic acid
e
28.57 53.84 22.22 22.22 39.21
Cefoxitin
a,b
0 7.69 0 0 3.92
Aminoglycosides
Gentamycin
b
14.28 11.53 0 0 7.84
Kanamycin
b
14.28 11.53 0 0 7.84
Fluoroquinolone Ooxacin
d
28.57 23.07 33.33 44.44 29.41
Macrolides Erythromycin
d
28.57 30.76 33.33 33.33 31.37
Tetracylin Tetracyclin
f
57.14 61.53 44.44 44.44 54.90
Sulfonamides
Sulfamide
g
57.14 69.23 55.55 66.66 64.70
Sulfamide/triméthoprime
c
28.57 15.38 22.22 11.11 17.64
Phenicols Chloramphénicol
a,b
0 0 22.22 11.11 5.88
Fosfomycine
Fosfomycin
a
0 0 11.11 0 1.96
a,b,c,d,e,f,g,h
: signicant dierence (P<0.05)
_____________________________________________________________________________Revista Cientifica, FCV-LUZ / Vol. XXXIV, rcfcv-e34389
5 of 8
Resistance assessment of isolated E. coli strains showed that
72.55% of strains were multiresistant as dened by CLSI [36], 15.67%
were double–resistant, 5.88% were resistant to a single antibiotic and
5.88% were susceptible to all antibiotics assessed. Multi–resistant
strains present a medical hazard, because in the event of human
or animal infection, it will be dicult to obtain satisfactory results
without the prior use of antibiotic susceptibility testing, especially as
these strains can cause food poisoning and/or dangerous foodborne
infections. This multiple antibiotic resistance is mainly due to
unregulated use in humans, animals, and agriculture [37, 38].
The E. coli strains isolated showed high levels of resistance to
penicillin (86.27%), ampicillin (82.35%) and, to a lesser extent,
sulfonamides (64.70%). This resistance is due to their availability
on the market and their frequent use on farms at the slightest sign
of possible disease, especially by breeders. Some of the authors have
also reported high rates of resistance for these antibiotics, ranging
from 70 to 100% resistance for E. coli isolated from milk and meat,
notably in Algeria [39, 40, 41], Mexico [28] and Brazil [42]. Lower
resistance rates are reported in Bangladesh [32].
A resistance of 39.21% was observed for amoxicillin associated
with clavulanic acid, in Algeria, lower prevalences of resistance are
reported [25, 39, 41] for E. coli strains isolated from milk and meat, but
also, high resistance prevalences are reported by Dib et al. [40], as
well as Abimbola et al. 2023 (98.1%) [43] in Nigeria, Martínez–Vázquez
et al. [28] (100%) in Mexico and Hussein et al. (2023) [44] (76%) in
Lebanon, having worked on cheese.
This results are close to those reported by Worku et al. [45] in
Ethiopia, and by Obaidat et al. [46] in Jordan in imported beef. In
Algeria, this antibiotic is being used exclusively in humans, especially
children, and is included in the list of medicines subject to compulsory
medical prescription, for this reason it cannot be ruled out that this
contamination is of human origin, either directly during processing
or indirectly at farm level.
For Ooxacin, resistances far exceeding these results (29.41%) are
reported in Algeria [39, 41], Uganda [47] and Sri Lanka [30] for strains
isolated from various white and red meats, and milk. This results
are close to those reported in Morocco [27] in chicken products,
Bangladesh [32] in frozen chicken and Jordan [46] in imported
beef. Lower levels of resistance have been reported in Algeria [25],
Mexico [28] and Lebanon [44] for strains isolated from cheese. These
resistances are due to the use of quinolones in poultry farming [30]
and signicantly in Africa [37].
Erythromycin resistance is 31.37%, resistance rates of 60, 98.72
and 100% reported in Bangladesh [48], Algeria [40] and Saudi
Arabia [49], respectively, in contrast to those reported in Morocco
with a resistance rate of 1% [27] for E. coli strains isolated from
chicken products. Erythromycin is the antibiotic of choice used by
veterinarians for respiratory deseases in Algeria, and failure to comply
with rearing conditions leads to repeated respiratory ailments and
repeated use of this antibiotic, which will result in prominent levels
of resistance throughout the country in the years to come.
For oxytetracycline, 54.90% resistance is reported, this results
are close to those reported in Algeria by Boudjerda and Lahouel [25]
(64.25%), in Ethiopia by Asfaw et al. [50] (52.5%), in Bangladesh by
Hossain et al. [32] (66%) and in Mexico by Martínez–Vázquez etal.
[28] (60%). However, lower resistance rates than these results were
reported in Algeria [40, 41] and Morocco for chicken meat products
[27]. Aberkan et al. [39] and Boudjerda and Lahouel (2015) [51]
reported resistance of 100 and 96.41% in Algeria, respectively, as
did Worku et al. (2022) [45] (100%) in Ethiopia. These resistances
are due to overuse of this antibiotic, taking into account the fact
that in 2016, oxytetracycline accounted for 63% of the antibiotic
used in Africa [37].
An exceptionally low resistance rates were found for Cefoxitin
(3.92%), Gentamycin (7.84%), Kanamycin (7.84%), Sulfonamides
associated with Trimethoprim (17.64%), Chloramphenicol (5.88%) and
Fosfomycin (1.96%), these results are close to those reported in Algeria
[39, 41]. This low level of resistance can be explained by the fact that
these antibiotics are unfamiliar to breeders, less used by veterinarians
and doctors, unavailable in pharmacies and only for hospital use in
injectable form, or completely banned like chloramphenicol.
However, some Algerian authors who have isolated E. coli from
chicken meat have reported high resistance rates for some of these
antibiotics [40, 51], which are worrying, especially with the irrational
and clandestine use of certain banned antibiotics in Algeria.
CONCLUSIONS
Food safety, food processing and antibiotics, all of it, represent
risks for public health, and concern all human beings, which arise
the importance of adopting “One Health” concept and the necessity
of implementing national and international programs, conventions,
and aids in developing countries.
Our results show a low level of hygiene in meat produced and marketed
in the Souk Ahras region, and indicate a high risk for consumers.
This type of meat also represents a potential reservoir for multidrug
resistant E. coli, which can be transferred to humans and cause
poisoning and/or infections.
The application of good production and hygiene practices
throughout the food chain is becoming an absolute necessity, as is
the training and awareness–raising of professionals in the sector, and
the provision of information to consumers. This will help reduce the
number of illnesses caused by these meats, and curb the spread of
multi–resistant strains, which are becoming increasingly worrying.
Conicts of interest
The authors declare no conict of interest.
BIBLIOGRAPHIC REFERENCES
[1] Moosavy MH, Kordasht HK, Khatibi S, Sohrabi H. Assessment of
the chemical adulteration and hygienic quality of raw cow milk
in the northwest of Iran. Qual. Assur. Saf. Crop Foods. [Internet].
2019; 11(5):491–498. doi: https://doi.org/m7f2
[2] Forsythe SJ. The Microbiology of Safe Food. 3rd ed. Hoboken
(NJ, USA): Wiley–Blackwe;ll; 2020. 608 p.
[3] FAO; IFAD; UNICEF; WFP; WHO. The State of Food Security and
Nutrition in the World 2023. Urbanization, agrifood systems
transformation and healthy diets across the rural–urban
continuum [Internet]. Rome: FAO; IFAD; UNICEF; WFP; WHO;
2023. 316 p. doi: https://doi.org/gtsdxk
Hygienic quality of food from animal origin and antibiotic resistance / Tamendjari et al. ____________________________________________
6 of 8
[4] Codex Alimentarius Commission. WHO Global strategy for
Food Safety 2022–2030 – update of status. Joint FAO/WHO
food standards programme. Forty–fourth Session [Internet].
Rome: FAO; WHO; 2023 [cited 08 Jan 2024]. 3 p. Available in:
https://goo.su/DeErUzU
[5] Clinical and Laboratory Standard Institute (CLSI). Performance
standards for antimicrobial susceptibility testing; 25th
Informational Supplement. Wayne (Pennsylvania, USA): CLSI;
2015; 231 p. (CLSI Supplement M100–S25)
[6] International Organization for Standardization. ISO 17604:2015.
Microbiology of the food chain—Carcass sampling for microbiological
analysis. 2nd ed. Geneva (Switzerland): ISO; 2015. 13 p.
[7] International Organization for Standardization. ISO 6887–1:2017.
Microbiology of the food chain—Preparation of test samples,
initial suspension and decimal dilutions for microbiological
examination. Part 1: General rules for the preparation of the initial
suspension and decimal dilutions. 2
nd
ed. Geneva (Switzerland):
ISO; 2015. 26 p.
[8] Guiraud JP. Microbiologie alimentaire. Paris: DUNOD; 1998. 652p.
[9] International Organization for Standardization. ISO 7218:2007.
Microbiology of food and animal feeding stuffs—General
requirements and guidance for microbiological examinations
3rd ed. Geneva (Switzerland): ISO; 2007. 66 p.
[10] Marques de Sá JP. Applied Statistics Using SPSS, STATISTICA,
MATLAB and R. 2
nd
ed. Helderberg (Germany): Springer; 2007. 505p.
[11] Ghazi K, Niar A. [Hygienic Quality of Cow Milk, in Various Bovine
Breeds of Tiaret Area (Algeria)].Tropicultura. [Internet]. 2011
[cited 19 Dec 2023]; 29(4):193–196. French. Available in: https://
goo.su/Az8AC
[12] Aggad H, Mahouz F, Ahmed Ammar Y, Kihal M. [Assessment
of milk hygienic quality in western Algeria]. Rev. Méd. t.
[Internet]. 2009 [cited 19 Dec 2023]; 160(12):590–595. Available
in: https://goo.su/tPrJOo1
[13] Hamiroune M, Berber A, Boubekeur S. [Bacteriological quality
of raw milk from local and improved cows in the region of Jel
and Blida (Algeria) and impact on public health]. Ann. Méd. Vét.
[Internet]. 2014 [cited 8 Apr 2023]; 158(2):137–144. French.
Available in: https://bit.ly/46MS9vf
[14] Ministry of Commerce. Interministerial Decree of 2 Moharram
1438 corresponding to 4 October 2016, setting the microbiological
criteria for foodstuffs. Ocial Journal of the Republic of Algeria
[Internet]. 2017 [cited 19 Dec 2023]. 39:11–32. Available in:
https://bit.ly/3NhGJsh
[15] Fereja AB, Aboretugn NF, Bulti NQ. Determination of microbial
hygiene indicators of raw cow milk in Assosa district, Ethiopia. J.
Food Qual. [Internet]. 2023; 2023:6769108. doi: https://doi.org/m7jr
[16] Mannani M, Ariri N, Bitar A. Microbiological and physicochemical
quality of raw milk of Beni Mellal–Khenifra. Rocz. Panstw. Zakl.
Hig. [Internet]. 2023;74(3):265–274. doi: https://doi.org/m7js
[17] Bacigale SB, Ayagirwe RB, Mutwedu VB, Mugumaarhahama
Y, Mugisho JZ, Nziku Z, Fofana M, Udomkun P, Mignouna J.
Assessing milk products quality, safety, and inuencing factors
along the dairy value chain in eastern Democratic Republic of
the Congo. Front. Sustain. Food Syst. [Internet]. 2023; 7:1105515.
doi: https://doi.org/m7jt
[18] Vignola CL; Fondation de technologie laitière du Québec.
Sciences et technologie du lait. Montréal (Canada): Presses
internationale Polytechnique; 2002. Chapitre 6, Classication
des principaux microorganismes du lait; p. 89–91.
[19] Guergueb N. The hygienic quality of raw milk intended for human
consumption in Algeria: Meta–analysis. Rev. Cient. FCV–LUZ.
[Internet]. 2024; 34(1):e34301. doi: https://doi.org/m7k5
[20] Harhoura Kh, Boukhors KT, Dahmani A, Zenia S, Aissi M.
Survey of hygiene in ovine slaughterhouses of Algiers region
by bacteriological analysis of carcasses. Afr. J. Microbiol. Res.
[Internet]. 2012 [cited 19 Dec 2023]; 6(22):4722–4726. Available
in: https://goo.su/shSDFn8
[21] Jaja IF, Green E, Muchenje V. Aerobic Mesophilic, Coliform,
Escherichia coli, and Staphylococcus aureus counts of raw meat
from the formal and informal meat sectors in South Africa. Int.
J. Environ. Res. Public Health. [Internet]. 2018; 15(4):819. doi:
https://doi.org/gdvt7j
[22] Djenidi R. Étude de la contamination supercielle des carcasses
ovines à l’aide d’examens bactériologiques au niveau de l’abattoir
de Bordj Bou Arréridj [Study of surface contamination of sheep
carcasses by bacteriological examinations at the Bordj Bou
Arréridj slaughterhouse]. Rev. Agric. [Internet]. 2016 [cited 22
Dec 2023]; 7(2):47–56. Available in: https://goo.su/aAl0w
[23] Nouichi S, Hamdi TM. Supercial bacterial contamination of
ovine and bovine carcasses at El–Harrach slaughterhouse
(Algeria). Eur. J. Sci. Res. [Internet]. 2009 [cited 19 Dec 2023];
38(3):474–485. Available in: https://goo.su/Xf5y
[24] El Hadef–El Okki S, El–Groud R, Kenana H, Quessy S. [Assessment
of supercial contamination of bovine and ovine carcasses
from the municipal slaughterhouse of Constantine]. Can. Vet.J.
[Internet]. 2005 [cited 23 Dec 2023]; 46(7):638–640. Available
in: https://goo.su/vs9S
[25] Boudjerda D, Lahouel M. Virulence and antimicrobial resistance
of Escherichia coli isolated from chicken meat, beef, and raw
milk. Austral J. Vet. Sci. [Internet]. 2022; 54(3):115–125. doi:
https://doi.org/m7nf
[26] Guergueb N, Alloui N, Ayachi A, Bennoune O. Effect of
slaughterhouse hygienic practices on the bacterial contamination
of chicken meat. Sci. J. Vet. Adv. [Internet]. 2014 [cited 23 Dec
2023]; 3(5):71–76. Available in: https://goo.su/qI9uH6o
[27] Fazza O, Favard Ennachachibi M, Ennassiri H, Hmyene A. Antibiotic
susceptibility of β–Glucuronidase–Positive Escherichia coli
isolated from poultry products in Morocco. Int. J. Food Sci.
[Internet]. .2023; 2023:7862168. doi: https://doi.org/m7ng
[28] Martínez–Vázquez AV, Mandujano A, Cruz–Gonzalez E, Guerrero
A, Vazquez J, Cruz–Pulido WL, Rivera G, Bocanegra–García V.
Evaluation of retail meat as a source of ESBL Escherichia coli
in Tamaulipas, Mexico. Antibiotics. [Internet]. 2022; 11(12):1795.
doi: https://doi.org/m7nh
_____________________________________________________________________________Revista Cientifica, FCV-LUZ / Vol. XXXIV, rcfcv-e34389
7 of 8
[29] Nobili G, La Bella G, Basanisi MG, Damato AM, Coppola R, Migliorelli
R, Rondinone V, Leekitcharoenphon P, Bortolaia V, La Salandra G.
Occurrence and characterisation of colistin–resistant Escherichia
coli in raw meat in southern Italy in 2018–2020. Microorganisms
[Internet]. 2022; 10(9):1805. doi: https://doi.org/m7nj
[30] Ranasinghe RASS, Satharasinghe DA, Anwarama PS,
Parakatawella PMSDK, Jayasooriya LJPAP, Ranasinghe RMSBK,
Rajapakse RPVJ, Huat JTY, Rukayadi Y, Nakaguchi Y, Nishibuchi
M, Radu S, Premarathne JMKJK. Prevalence and antimicrobial
resistance of Escherichia coli in chicken meat and edible poultry
organs collected from retail shops and supermarkets of North
Western province in Sri Lanka. J. Food Qual. [Internet]. 2022;
2022:8962698. doi: https://doi.org/m7nk
[31] Klaharn K, Pichpol D, Meeyam T, Harintharanon T, Lohaanukul P,
Punyapornwithaya V. Bacterial contamination of chicken meat in
slaughterhouses and the associated risk factors: A nationwide
study in Thailand. Plos One. [Internet]. 2022; 17(6):e0269416.
doi: https://doi.org/m7nm
[32] Hossain MMK, Islam MS, Uddin MS, Rahman ATMM, Ud–Daula
A, Islam MA, Rubaya R, Bhuiya AA, Alim MA, Jahan N, Li J, Alam
J. Isolation, identification and genetic characterization of
antibiotic resistant Escherichia coli from frozen chicken meat
obtained from supermarkets at Dhaka city in Bangladesh.
Antibiotics. [Internet]. 2022; 12(1):41. doi: https://doi.org/m7nq
[33] Akermi A, Ould A, Aggad H. Bacteriological status of chicken meat
in western Algeria. Lucr. Ştiinţ. Med. Vet. [Internet]. 2020 [cited
23 Dec 2023]; 53(2):5–13. Available in: https://goo.su/hytqH
[34] Eyi A, Arslan S. Prevalence of Escherichia coli in retail poultry
meat, ground beef and beef. Med Weter. [Internet]. 2012 [cited
23 Dec 2023]; 68(4):237–240. Available in: https://goo.su/Fd9VO
[35] Fédération du Commerce et de la Distribution. Critères
microbiologiques applicables à partir de 2020 aux marques de
distributeurs, marques premiers prix et matières premières dans
leur conditionnement initial industriel. France. [Internet]. 2020
[cited 19 Dec 2023]; 61 p. French. Available in: https://goo.su/CTwR
[36] Clinical Laboratory Standards Institute (CLSI). Performance
standards for antimicrobial susceptibility testing; 15th
informational supplement. Wayne (Pennsylvania, USA): CLSI;
2008. 22 p. (CLSI Supplement M100–S15).
[37] Mshana SE, Sindato C, Matee MI, Mboera LEG. Antimicrobial
use and resistance in agriculture and food production systems
in Africa: a systematic review. Antibiotics. [Internet]. 2021;
10(8):976. doi: https://doi.org/gqdb26
[38] Schar D, Sommanustweechai A, Laxminarayan R,
Tangcharoensathien V. Surveillance of antimicrobial consumption
in animal production sectors of low – and middle–income countries:
Optimizing use and addressing antimicrobial resistance. PLoS
medicine. [Internet]. 2018; 15(3):e1002521. https://doi.org/gpcwf7
[39] Aberkane C, Messaï A, Messaï CR, Boussaada T. Antimicrobial
resistance pattern of avian pathogenic Escherichia coli with
detection of extended–spectrum β–lactamase–producing
isolates in broilers in east Algeria. Vet World. [Internet]. 2023;
16(3):449–454. doi: https://doi.org/mxzq
[40] Dib AL, Chahed A, Lakhdara N, Agabou A, Boussena S, Ghougal K,
Lamri M, Sana Kerrour N, Kadja L, Bouaziz A, Benmerzoug M, Ousaad
L, Mezouani O, Moreno E, Espigares E, Gagaoua M. Preliminary
investigation of the antimicrobial and mechanisms of resistance
of Enterobacteria isolated from minced meat in the Northeast of
Algeria: The case of butchers from Constantine. Integr. Food Nutr.
Metab. [Internet]. 2019; 6:1–7. doi: https://doi.org/m7pw
[41] Agabou A, Lezzar N, Ouchenane Z, Khemissi S, Satta D, Sotto A,
Lavigne JP, Pantel A. Clonal relationship between human and
avian ciprooxacin–resistant Escherichia coli isolates in North–
Eastern Algeria. Eur. J. Clin. Microbiol. Infect. Dis. [Internet].
2016; 35(2):227–234. doi: https://doi.org/m7px
[42] Furlan JPR, Gallo IFL, de Campos ACLP, Passaglia J, Falcão JP,
Navarro A, Nakazato G, Stehling EG. Molecular characterization
of multidrug–resistant Shiga toxin–producing Escherichia coli
harboring antimicrobial resistance genes obtained from a
farmhouse. Pathog. Glob. Health. [Internet]. 2019; 113(6):268–
274. doi: https://doi.org/m7pz
[43] Owoseni AA, Adigun TO, Asogbon OH, Atobatele BO, Adeleke OA,
Nejo YT. Presence of antibiotic resistance genes in bacteria isolated
from raw cow milk obtained from Bowen University Dairy Farm
[Internet]. IOP Conference Series: Earth Environmental Science.
International Conference on Sustainable Dairy Production; 2022
Nov 28 – Dec 01; Bowen University, Iwo (Nigeria). Bristol (GB): IOP
Publishing Ltd; 2023. 10 p. doi: https://doi.org/m7p2
[44] Hussein ND, Hassan JW, Osman M, El–Omari K, Kharroubi
SA, Toufeili I, Kassem II. Assessment of the microbiological
acceptability of white cheese (Akkawi) in Lebanon and the
antimicrobial resistance proles of associated Escherichia coli.
Antibiotics. [Internet]. 2023; 12(3):610. doi: https://doi.org/m7p4
[45] Worku W, Desta M, Menjetta T. High prevalence and antimicrobial
susceptibility pattern of Salmonella species and extended–
spectrum β–lactamase producing Escherichia coli from raw
cattle meat at butcher houses in Hawassa city, Sidama regional
state, Ethiopia. PLoS ONE. [Internet]. 2021. 17(1):e0262308. doi:
https://doi.org/m7p5
[46] Obaidat MM. Prevalence and antimicrobial resistance of Listeria
monocytogenes, Salmonella enterica and Escherichia coli O157:H7
in imported beef cattle in Jordan. Comp. Immunol. Microbiol.
Infect. Dis. [Internet]. 2020. 70:101447. doi: https://doi.org/m7p6
[47] Onohuean H, Igere BE. Occurrence, Antibiotic susceptibility
and genes encoding antibacterial resistance of salmonella
spp. and Escherichia coli from milk and meat sold in markets
of Bushenyi district, Uganda. Microbiol. Insights [Internet].
2022; 15:11786361221088992. doi: https://doi.org/m7p7
[48] Rahman MA, Rahman AKMA, Islam MA, Alam MM. Antimicrobial
resistance of Escherichia coli isolated from milk, beef and
chicken meat in Bangladesh. Bangl. J. Vet. Med. [Internet].
2017; 15(2):141–146. doi: https://doi.org/m7p9
[49] Hemeg HA. Molecular characterization of antibiotic resistant
Escherichia coli isolates recovered from food samples and
outpatient Clinics, KSA. Saudi J. Biol. Sci. [Internet]. 2018;
25(5):928–931. doi: https://doi.org/m7qb
Hygienic quality of food from animal origin and antibiotic resistance / Tamendjari et al. ____________________________________________
8 of 8
[50] Asfaw T, Genetu D, Shenkute D, Shenkutie TT, Amare YE,
Habteweld HA, Yitayew. Pathogenic bacteria and their antibiotic
resistance patterns in milk, yoghurt and milk contact surfaces
in Debre Berhan Town, Ethiopia. Infect. Drug Resist. [Internet].
2023; 16:4297–4309. doi: https://doi.org/m7qc
[51] Boudjerda D, Brugère H, Bibbal D, Lehouel M. Antibioresistance,
phylogeny and virulence markers of Escherichia coli strains
isolated from chicken meat commercialised in Jel Area (east
Algeria). Bulg. J. Agric Sci. [Internet]. 2016 [cited 19 Dec 2023];
22(3):505–512. Available in: https://goo.su/IDkBi