Introduction
The
non-judicious use of antimicrobial agents in poultry feed has been associated
with an increased incidence of antibiotic resistance (AR) in the microorganisms
of poultry origin. Commercial poultry farming is highly profitable because it
produces poultry meat with the least investment within 5‒6 weeks. Poultry farmers observe intense care in commercial broiler
farming, and particularly in the developing countries, such as Pakistan,
in-feed antibiotic drugs are prevalent for preventing a variety of poultry
diseases (Kamboh et al. 2018a). Although antibiotics are essential for
disease prevention and control, these have also found another use as growth
promoters in the poultry industry (Obajuluwa et al. 2021; Schwarz et
al. 2001). A number of recently published reports indicated that the meat
gained from the broilers reared on conventional antibiotic mixed feeds harbored
high counts of AR bacteria as compared to the one obtained from organically
reared chickens (Miranda et al. 2008a, b; Kamboh et al. 2018b).
The incidence of AR is a serious concern for human health because the use of
antimicrobial agents has been continuously increasing the types, strains, and
numbers of antibiotic-resistant bacteria (ARB). Since humans eat the poultry
products, including meat and eggs, the effectiveness of the antimicrobial
medicines which are used in poultry feed, has also reduced in human populations
(Asai et al. 2006; Caniça et al. 2019). Since the development of a novel group of
antimicrobial agents is really a challenging task (Ikele et al. 2020),
hence humans cannot afford their existing antimicrobial drugs to be inefficient
to control their diseases. The major reason for the increasing spread of AR is
unawareness of the masses about this problem. Hence research needs to be done
to provide conclusive evidence about the prevalence of AR in the sources of
human foods, particularly poultry meat.
Microbiota lives in the intestines of poultry birds
serve as their essential survivors against invading pathogens. Pathogenic
microorganisms, such as Escherichia coli, and Salmonella
compete with microbiota and cause diseases to poultry birds. E.
coli, a commensal bacterium, is globally considered a major reason for the
morbidity and mortality of humans and animals by causing food-borne infections
(Miskinyte et al. 2013; Khan et al. 2015). It can survive in
several hosts. Its pathogenicity and increase in AR have raised concerns
regarding community health and socioeconomic values (Pegues 2005). Moreover, Salmonella
is considered a growing threat to human health, as it exhibits highly deadly
pathogenic behavior in poultry birds. Moreover, Salmonella contaminates poultry meat and spreads infection in
humans through the consumption of infected poultry products (Nair and Johny
2019; Han et al. 2020).
Moreover, Salmonella is also a human pathogen that also enjoys poultry
as an alternate host. Two major species of Salmonella,
viz., Salmonella enterica and S.
bangori have been reported as sources of foodborne diseases in the US (CDCP
2013). There is a remarkably higher incidence of antibiotic-resistance in the
microbiota of chickens grown on diets containing antibiotic drugs as compared
to the ones reared without antimicrobial drugs (Zhang et al. 2011).
Similarly, lower AR bacteria are generally found in the organically grown
poultry birds in contrast to traditionally reared ones (Smith-Spangler et
al. 2012). The existing published reports used chicken as the model bird
for the prevalence and dissemination of AR in commercial and non-conventional
poultry farming systems but investigations in commercial and backyard/wild
quails are yet to be published.
The present study, therefore, used two
poultry models, i.e., commercial and
backyard/wild chickens and quails to elucidate the potential risks of AR. In
this study, the incidence of AR was explored in E. coli and Salmonella isolated from intestines and
meats of commercial and backyard/wild chickens and quails. The results
of this study will be beneficial for the poultry industry to understand the
perils of AR in commercial poultry, and provoke new research for the production
of antibiotic-free poultry.
Materials and Methods
Sample collection
Commercial and
backyard/wild chickens and quails were procured from a local live bird market
of Hyderabad, Sindh, Pakistan. The birds were assigned to four treatment
groups, i.e., C0: backyard
chickens, C1: commercial broiler, Q0: backyard/wild quails and Q1:
commercial quails. Each treatment group contained twenty birds (n=20 each). The
birds of each treatment group were exsanguinated using a sharp sterilized knife
on different days according to the requirements of the Directorate of Advanced
Studies, Sindh Agriculture University, Tandojam. The carcasses were eviscerated
and portioned using sterilized equipment. The cecal contents of each bird were
collected under aseptic conditions and stored in a laboratory freezer at
−24°C until required for analysis. The whole carcasses were subject to
chilling (4°C) after slaughter and analyzed for the isolation of pathogenic
microbes within 2 h.
Isolation of E.
coli and Salmonella
The isolation of two pathogenic microorganisms, including E. coli
and Salmonella, from the ceca, was
performed by
taking 1 g
samples, placing them in 9 mL of 0.9% sterile saline solution in a sterilized beaker, and vortexed. The samples were subsequently
diluted to prepare ten-fold dilution using the saline solution. About 1 mL of
each 10-fold diluted sample was cultured on the media, as described by Habib et
al. (2015).
On the other hand, the whole carcass was hand
rinsed under aseptic conditions in 100 mL of 0.85% sterile saline solution,
according to the method of Kilonzo-Nthenge et al.
(2008). About 25 mL of this solution was taken and mixed with 225 mL of 0.1%
peptone water. The samples were then incubated at 37°C for 24 h (pre-enrichment
culturing).
The sub-culturing of E. coli and Salmonella was done by
selecting the suspected bacteria and individually inoculating them onto
differential bacteriological agar media (Oxoid, Co., UK) under aseptic
conditions. The samples were incubated at 37°C for 12 h and pure cultures were
obtained. The conformation of bacterial species was performed according to the
method of Monica (1985).
Assessment of antibiotic resistance
The AR patterns of both the pathogenic isolates were verified according
to the protocol described by CLSI Guidelines (2012). Briefly, the AR of the
pathogenic bacterial (E. coli and Salmonella) isolates was assessed by the disk
dispersion method. The colonies of the pathogenic bacteria were added into
nutrient broth. The turbidity (0.5 McFarland
standard) of the broth was adjusted. These were spread on sensitivity
agar plates using sterile swabs. Subsequently, these were dried. In the next
step, the selected antibiotic discs of the antibiotic drugs were put on the
aforementioned sensitivity plates by maintaining an even distance. The amounts
of the antibiotic drugs were about 5 µg
for ciprofloxacin; 10 µg each for
ampicillin, gentamicin, and norfloxacin; 25 µg
for sulfamethoxazole; and 30 µg each
for chloramphenicol and oxytetracycline. Subsequently, these plates were
incubated at 37°C. The inhibition zones were measured after 24 h of the
incubation from the centre of the disc. The classification of AR breakpoints
was done using the protocol published by Lalitha
(2004), according to which the bacteria which had an inhabitation zone ≥ 21
mm were termed as ‘Susceptible’; those between 17–20 mm were
considered ‘Intermediate’; and the ones having ≤ 16 mm were classified
‘Resistants’. Multidrug-resistant (MDR) strains were those whose isolates
displayed resistance against 3 or more antibiotics (Kamboh et al.
2018b). The data for these parameters were collected in triplicate.
Statistical analysis
The general calculations and data analysis were performed using
Microsoft Excel (v. 2010). The comparison of the levels of AR between the four
treatment groups (P < 0.05) was performed by Fisher’s
exact test using JMP software (5.0.1.a, SAS, USA).
The
incidence of antimicrobial resistance
The data regarding AR of bacterial isolates
obtained from the backyard and commercial chickens and quails against 5 µg ciprofloxacin, 10 µg each of ampicillin, gentamicin,
neomycin, norfloxacin, 25 µg of
sulfamethoxazole, and 30 µg each of
chloramphenicol and oxytetracycline, and indicated significant differences (P
< 0.01) with only one
exception (Table 1). In this study, the comparison
between the treatment groups revealed that the bacterial isolates obtained from
both of the backyard chickens and quails exhibited significantly lower levels
of AR than those obtained from commercial birds against the eight antimicrobial
drugs tested in this study. The bacterial isolates obtained from the C1 group
exhibited the highest AR against each of ampicillin, ciprofloxacin, neomycin,
norfloxacin, sulfamethoxazole, and oxytetracycline. In contrast, the bacterial
isolates obtained from the Q1 group exhibited the highest AR against each of
the chloramphenicol, gentamicin in this study. On the other hand, the
comparison between the antibiotic drugs revealed that the highest levels of AR
in the bacterial isolates were observed against ampicillin for all the four
bird groups. Moreover, the second-worst results were observed against
gentamicin in C0, neomycin in each of C1 and Q0, and ciprofloxacin in Q1.
Finally, the lowest levels of AR of the bacterial isolates were observed
against norfloxacin in each of C0 and Q0, sulfamethoxazole in each of Q0 and
Q1, and chloramphenicol in C1.
The
resistance of E. coli against
antimicrobial drugs
The percentages of E. coli isolated from the intestines of
commercial and non-commercial chickens and quails selected in this study were
shown in Fig. 1. The criteria described by Lalitha
(2004) was used to classify the E. coli resistance against the
eight antimicrobial drugs, according to which the pathogen was susceptible to
the antibiotic drug if the inhibition zone on the disk was ≥ 21 mm,
whereas the pathogen was resistant to the drug if the inhibition zone was:
≤ 16mm, while the zone between 17–20 mm was considered intermediate. In
this study, the comparison between the treatment groups revealed that the E.
coli isolates of the commercial birds showed significantly higher
resistance than the backyard ones against all the tested antimicrobial drugs.
Moreover, the E. coli isolates of C1
exhibited a significantly (P < 0.01)
higher levels of AR than those of C0, whereas those of Q1 higher than those of
Q0. Furthermore, the E. coli isolates
of C1 exhibited higher levels of AR than those of Q1 against five drugs
(ampicillin, neomycin, norfloxacin, sulfamethoxazole, and oxytetracycline), but
lower against two drugs (gentamicin and chloramphenicol). On the other hand,
the comparison between the antibiotic drugs revealed that the E. coli isolates exhibited the highest
levels of AR against ampicillin in all the four treatment groups. Finally, the E. coli isolates exhibited the lowest
levels of AR against gentamicin in C1, and against sulfamethoxazole in Q1.
However, the E. coli isolates of
backyard chickens showed the least resistance against four drugs
(ciprofloxacin, neomycin, norfloxacin, and sulfamethoxazole). Finally, the E. coli isolates of backyard quails
exhibited no resistance against four drugs (ciprofloxacin, norfloxacin,
chloramphenicol, and oxytetracycline) in this study.
The
resistance of Salmonella against antimicrobial drugs
The data regarding the percentages of Salmonella isolates obtained from the intestines of commercial and
non-commercial chickens and quails selected in this study were shown in Fig. 2.
The isolates obtained from commercial birds exhibited significantly (P < 0.01) higher AR than those isolated
from non-commercial ones against all the tested antimicrobial drugs. Moreover,
the Salmonella isolates of C1 exhibited significantly higher levels of
AR than those obtained from C0, whereas those of Q1 higher than those of Q0.
Furthermore, the Salmonella isolates of C1 exhibited higher levels of AR
than those of Q1 against all the tested antimicrobial drugs in this study. On
the other hand, the comparison between the antibiotic drugs revealed that the Salmonella
isolates exhibited the highest levels of AR against ampicillin in all the four
bird groups. Moreover, the Salmonella isolates exhibited the least of AR
against two antimicrobial drugs including gentamicin and chloramphenicol in Q1.
Furthermore, the isolates of both the commercial bird types (C1 and Q1) showed
the lowest resistance against chloramphenicol. Finally, the Salmonella isolates obtained from
backyard chickens and quails exhibited no resistance against norfloxacin and
sulfamethoxazole, respectively in this study.
Multidrug
resistance patterns
Table 1: Overall percentages of bacterial isolates of commercial
and non-commercial poultry resistant to antimicrobial agents
|
Antimicrobials |
µg |
C0 n=44 |
C1 n=64 |
Q0 n=44 |
Q1 n=56 |
||||
|
# |
% |
# |
% |
# |
% |
# |
% |
||
|
Ciprofloxacin |
5 |
5 |
11.36 |
44 |
68.75 |
1 |
2.27 |
38 |
67.86 |
|
Ampicillin |
10 |
14 |
31.82 |
56 |
87.50 |
6 |
13.64 |
44 |
78.57 |
|
Gentamicin |
10 |
8 |
18.18 |
35 |
54.69 |
3 |
6.82 |
35 |
62.50 |
|
Neomycin |
10 |
6 |
13.64 |
52 |
81.25 |
4 |
9.09 |
34 |
60.71 |
|
Norfloxacin |
10 |
3 |
6.82 |
41 |
64.06 |
1 |
2.27 |
34 |
60.71 |
|
Sulfamethoxazole |
25 |
5 |
11.36 |
43 |
67.19 |
1 |
2.27 |
32 |
57.14 |
|
Chloramphenicol |
30 |
7 |
15.91 |
35 |
54.69 |
2 |
4.55 |
33 |
58.93 |
|
Oxytetracycline |
30 |
6 |
13.64 |
49 |
76.56 |
2 |
4.55 |
33 |
58.93 |
C0: backyard chickens; C1:
commercial broiler; Q0:
backyard/wild quails; Q1:
commercial quails (P Value < 0.001 for all antimicrobials)
%2052-59_files/image002.png)
Fig. 1: Percentages of Escherichia
coli isolated from commercial and non-commercial poultry susceptible (S),
intermediate (I) and resistant (R) to antimicrobial agents by disk diffusion method. C0: backyard chickens (n=28); C1:
commercial broiler (n=40); Q0: backyard/wild quails (n=24); Q1: commercial quails (n=36)
The data regarding the prevalence of MDR in
the two bacterial isolates obtained from commercial and backyard poultry were
summarized in Fig. 3. The percentages of MDR E. coli and Salmonella
isolates of commercial birds (95 and 77% for C1 and Q1) were significantly
higher (P = 0.0082 and 0.0076,
respectively) than those obtained from non-commercial ones (67.8 and 54.2% for
C0 and Q0). Similarly, the levels of MDR Salmonella isolates of
commercial birds (92.8 and 85% for C1 and Q1) were higher (P = 0.0266 and 0.0060, respectively) than their counterparts
obtained from the backyard birds (81.2 and 60% for C0 and Q0). The best results
were shown by Q0, for which 45.8 and 40% E. coli and Salmonella isolates showed the
resistance against 0–1 antimicrobial drugs, whereas
the worst results were shown by C1, for which 42.8 and 28.6% E. coli and
Salmonella isolates showed the
resistance against > 6 antimicrobial drugs.
Discussion
Food-borne pathogens have become a leading threat to public health
throughout the world. These include E.
coli, Salmonella, Shigella, and Campylobacter, while raw and partially-cooked
poultry meat products harbor them the most. Particularly, Salmonella and E. coli
proliferate to human populations during the handling of untreated poultry
carcasses, as well as through consumption of partially or improperly cooked
poultry products (Chen et al. 2020). Another rising threat to human
beings is the incidence of AR microorganisms, for which leading cause has been
thought to be the non-judicious use of antibiotic drugs in the poultry feed. A
recently published report suggested that in the European countries the E.
coli isolates obtained from poultry and cattle exhibited greater resistance
to antimicrobial drugs, and there were very strong associations between the
dosages of antibacterial drugs and their patterns of antibiotic resistance (Chantziaras
et al. 2013; Ariffin et al. 2019). Moreover, FDA has highlighted
that the resistance against antimicrobial drugs in the Enterobacteriaceae family
can be transferred from poultry reared on those antimicrobial drugs to human
populations (Rafiei and Nasirian 2003), particularly through the
consumption of eggs, milk, and meat obtained from such animals and poultry
birds (Reig and Toldra 2008).
%2052-59_files/image004.png)
Fig.
2: Percentages of Salmonella isolated from commercial and
non-commercial poultry susceptible (S), intermediate (I) and resistant (R) to
antimicrobial agents by disk diffusion method. C0: backyard
chickens (n=16); C1: commercial broiler (n=24); Q0: backyard/wild quails (n=20);
Q1: commercial quails (n=20)
%2052-59_files/image006.png)
Fig. 3: Percentage
of Escherichia coli and Salmonella
isolates of commercial and
non-commercial poultry resistant to multiple antimicrobials. C0: backyard chickens; C1: commercial broiler; Q0: backyard/wild quails; Q1: commercial quails
The primary purpose of using antibiotic drugs
in poultry feed and water is to prevent diseases in the commercial flocks.
However, owing to the enhanced feed efficiency and weight gain with these
drugs, their non-judicious use up to unacceptable levels has increased to
achieve maximum monetary benefits from the commercial poultry flocks. Recently
published reports have suggested that the non-medical use of these drugs
results in rendering these drugs ineffective against the control of few strains
of gut microbes, which upon poultry harvest can be transferred to the human
food chain (Koga et al. 2015).
Our previously results (Kamboh et al. 2018b) and findings of some other
authors (Miranda and Zemelman 2002; Nisar
et al. 2017; Davis et al. 2018; Gad et al. 2018) suggest
that the incidence of AR microbes was higher in commercially reared chickens as
compared with those in domestically reared ones. In this study, the E. coli and Salmonella isolates obtained from the commercial broiler chickens
and quails exhibited alarmingly higher resistance patterns against the eight
antibiotic drugs tested in this experiment, as compared with the isolates
obtained from backyard chickens and wild quails. In previously published
studies, poultry reared without antibiotics reported less antibiotic-resistant E.
coli as compared with the conventionally reared ones (Zhang et al.
2011). Similarly, the chicks reared on an organic diet have also been found to
have lower numbers of antibiotic-resistant bacteria than those reared on a
commercial diet (Smith-Spangler et al. 2012).
Unfortunately, during the last two decades,
the nonjudicial use of antibiotics for seeking higher profitability in the
poultry sector has tremendously increased in most of the countries having poor
economic conditions. Particularly in Pakistan, the increase in the use of
antibiotics has been about 65% in the last 16 years in the poultry sector
(Klein et al. 2018). The major reason associated with nonjudicial infeed
consumption of antibiotics for poultry production includes poor rearing
conditions, high microbial contamination in feed and drinking water, imbalanced
poultry nutrition, increasing occurrences of urbanization-related nonbacterial
infections, which have caused to increased prevalence of AR of pathogenic bacteria
(Weaver 2013; Collineau et al. 2017; Nandi et al. 2017; Klein et
al. 2018). Particularly, in this report, all the bacterial isolates showed
high resistance (about 54%) against chloramphenicol. It is an antibiotic drug
that has been banned for use in the poultry diet in several countries such as
Europe and the US; however, it is still excessively being used in several
developing countries.
Moreover, the findings of this study revealed
that the commercial broiler chickens and quails exhibited a higher incidence of
MDR strains of both E. coli and Salmonella than those of non-commercial
chickens and quails. These findings agreed to the results of Miranda et al.
(2008a), who found a higher incidence of MDR enteric microbes in the meat
obtained from commercially reared chickens (63.3%) as compared with those
obtained from turkeys (56.7%) and organic chickens (41.7%) after the
application of aminoglycosides, penicillins, and quinolones in the diets of
commercial chicks. Extensive and non-judicial use of antibacterial agents in
the poultry feeds makes Salmonella
and E. coli become resistant
against those drugs (Fielding et al. 2012). The phenomenon of MDR against
the antimicrobial drugs investigated in this study was in agreement with the
earlier published report (Brown et al. 2019).
Several studies have investigated the role of
antimicrobial drugs in the poultry production systems in the induction of AR in
poultry birds (Chantziaras et al. 2013; Kamboh et al. 2018b).
Moreover, several reports have published the resistance patterns of pathogenic
microbial isolates obtained from poultry being reared in the organic and
conventional production systems (Miranda et al. 2008b; Miranda et al.
2009). It has been well documented that the zoonotic microorganisms isolated
from conventional poultry production systems exhibit a remarkably higher
prevalence of AR in contrast to the ones isolated from organic production
systems (Young et al. 2009). Particularly, the isolates of E. coli obtained from conventional and
organic production systems exhibited similar AR patterns in a European study (Österberg et al. 2016). Similarly, some other
reports also found that the isolates of E.
coli and Staphylococcus aureus
from beef (Miranda et al. 2009) and intestines (Sato et al. 2004,
2005) obtained from conventional rearing system exhibited higher antimicrobial
resistance in contrast to the ones obtained from an organic production system.
Furthermore, the phenomenon of multidrug resistance was also higher in the
bacterial isolates of the liver obtained from commercial broilers as compared
to those of backyard chickens (Kamboh et al. 2018b).
The
AR of both the bacterial isolates (E.
coli and Salmonella)
obtained from commercial broiler chickens and quails were higher in contrast to
those of their non-commercial counterparts against the eight antimicrobial
drugs tested in this study. Moreover, the total bacterial (E. coli and Salmonella) isolates obtained from all
the four bird groups were the most resistant against ampicillin, followed by
neomycin in this study. Finally, the incidence of MDR in both bacteria was also
higher in the commercial chickens and quails isolates as compared with their
non-commercial backyard counterparts.
Acknowledgements
Authors are highly thankful
to Central Veterinary Diagnostic Laboratory (CVDL) Tandojam for providing
facilities to carry out this work.
Authors Contributions
Asghar Ali Kamboh
conceptualized the study, Asghar Ali Kamboh and Tarique Ali Rind performed the
research. Muhammad Amar Khan wrote the manuscript, and Kanwar Kumar Malhi
contributed to analysis and interpretation of the study data. Rehana Burriro and Riaz Ahmed Leghari helped in analysis and proof
reading.
Conflict of interest
The authors declare that they have no
conflict of interest.
Data availability
All data reported in this article are available and will be
produced on demand.
Ethics Approval
All study protocols were approved by
the Directorate of Advanced Studies, Sindh Agriculture University, Tandojam.
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