Introduction
Non-typhoidal
Salmonella is one of the important
zoonotic pathogens affecting both humans and animals is also considered the
leading cause of bacterial diarrhea in the entire world. An estimated 153
million cases and 57000 deaths of nontyphoidal human salmonellosis are reported
every year worldwide (Brunette 2017; Sharma et al. 2019). The majority of
human cases of non-typhoidal Salmonella are foodborne. Infection caused by non-typhoidal Salmonella is usually self-limiting and in most cases,
antimicrobial treatment is not required.(Angulo et al. 2000). However antimicrobial resistance is relevant in 3‒10% of cases where the infection is caused by invasive
strains resulting in bacteremia and life-threatening conditions particularly in
young and immunocompromised individuals (Okeke et al. 2005; Chen et al. 2013).
The rise of antimicrobial resistance is a growing
public health issue worldwide due to extensive use in agriculture, food and
veterinary medicine which need to be controlled at the international level (De
Oliveira et al. 2005). The
development of Multi-Drug Resistance among foodborne pathogens is increasing
dramatically all over the world and among these AMR in Salmonella is a serious emerging issue (Bronzwaer
et al. 2002; Chen et al. 2013; Eng
et al. 2015). Zoonotic non-typhoidal Salmonella
has the properties of acquiring antimicrobial resistance over the years (Michael
and Schwarz 2016). However the rate of antimicrobial resistance varies with
different antibiotics and serotypes and Salmonella
enterica serovar Enteritidis followed by
Salmonella Typhimurium is
relatively more susceptible to antimicrobial resistance than others, is one of
the most prevalent serotypes (Su et al
2004; Chen et al. 2013). A much
higher rate of antibiotic resistance is also found in, another important
serovar prevalent worldwide Centers for Disease Control and Prevention consider
MDR Salmonella a serious public
health threat that should be controlled efficiently on an urgent basis to avoid
aggravated circumstances. Conventional antimicrobial agents such as
sulphamethoxazole, chloramphenicol, ampicillin and trimethoprim are used as
traditional first-line treatments for treating Salmonella. Salmonella enterica
spp which are resistant to conventional antimicrobials are denoted as
multidrug-resistant (MDR) Salmonella
(Su et al. 2004; Eng et al. 2015; Bugarel et al. 2017). Resistance to the
second-line treatment including fluoroquinolones which were used as a choice of
treatment in MDR regions has also been reported (Chau et al. 2007; Klemm et al.
2018). Antimicrobial resistance both in typhoidal and non-typhoidal Salmonella is increasing in developing
countries particularly the Indian subcontinent and Southeast Asia due to
extensive use of antibiotics in public hospitals and communities (Threlfall
2002; Sharma et al. 2019). This
situation is even grimmer in middle and low-income countries like Pakistan
where there is no law enforcement to control the overwhelming sale of
antibiotics. In Pakistan like our neighboring country, antibiotics are easily
available in pharmacies and anyone can purchase over the counter without the
prescription of health practitioners. (Sharma et al. 2019)
Until now in Pakistan, limited
data is available on the prevalence of zoonotic nontyphoidal Salmonella and its susceptibility to
different antimicrobial agents as compared to typhoidal Salmonella. A few studies have been reported on antimicrobial
resistance of Salmonella Enteritidis and Salmonella Typhimurium in
regions including Faisalabad (Akhtar et
al. 2010; Wajid et al. 2018), in
Sawat (Uddin et al. 2018) and Karachi
(Shah and Korejo 2012).
The objective of this study was
to check antimicrobial resistance in Salmonella
Enteritidis and Salmonella Typhimurium
isolated from different sources of the poultry food chain and humans in Lahore.
Materials and
Methods
A cross-sectional study was conducted from 2017‒2019 and samples were collected from different steps of the
broiler meat production chain. Isolates from different sources including human,
food and, the environment were used For the present study, a total of 71 Salmonella strains (Salmonella Typhimurium, n=45; Salmonella
Enteritidis, n =26) were included for antimicrobial susceptibility testing (Table
1).
All Salmonella
isolates were initially confirmed by biochemical tests. Salmonella serovar Typhimurium
and Enteritidis and were
confirmed through PCR by targeting their specific spy and, sdf genes, respectively (Alvarez et al.
2004).
Antimicrobial
susceptibility testing by disc diffusion method
Antimicrobial susceptibility testing was performed by
Kirby-Beur disc diffusion method according to Clinical and Laboratory Standards
Institute (CLSI) guidelines. The antibiotics which are commonly used in poultry
production were selected and purchased. The antibiotics disks (OXOID, Thermo
Scientific Ltd). and their concentration (microgram) used were, ampicillin 25
(AMP), amoxicillin 10 (AML), gentamicin 10 (CN), streptomycin 10 (S),
ciprofloxacin 5 (CIP), nalidixic acid 30 (NA), trimethoprim 5 (W), tetracycline
30 (TE), sulphafurazole 300 (SF) and chloramphenicol 30 (C).
Refreshing of isolates and
preparation of inoculum
Purified preserved cultures of Salmonella Typhimurium
and Salmonella Enteritidis were refreshed in 10 mL tryptone soy broth with an
overnight incubation at 37ºC. A loopful of the bacterial isolate was then
streaked on nutrient agar plates and incubated for 24 h at 37ºC. Four to five
well isolated and purified colonies were picked from plates with sterilized
loop and properly mixed in test tubes containing 10 mL phosphate buffer saline.
The turbidity of bacterial culture was standardized at 0.5 McFarland (CLSI
2005). Another test tube containing 10 mL of PBS solution without inoculum was
used as blank.
Approximately
20 mL of Mueller-Hinton agar (OXOID, Ltd) medium was poured into 90 mm
diameter sterile Petri dishes to a depth of 4 mm with overnight
incubation at 37°C to check for sterility (Kebede et al. 2016). After the adjustment of absorbance value, bacterial
culture was spread on the Mueller-Hinton agar (OXOID, Ltd ) plate within 15 min
with the help of a sterilized cotton swab. Briefly, the swab was dipped in a
culture mixture and excess liquid was removed by squeezing the swab on the
walls of the test tube. The swab was then streaked over the entire surface of the agar three
times by rotating the plate approximately 60º after each application to ensure
an even distribution of the inoculum. The plates were then allowed to dry for 5
min before the application of antibiotic discs. A total of five discs were
applied on a single plate for accurate measurement of the zones. The zones were
measured with a calibrated scale according to Clinical & Laboratory Standards Institute (CLSI)
guidelines.
Results
The
zones of inhibitions were measured according to the CLSI guidelines as
resistant and sensitive. Fig. 1
summarizes the Table 1: Salmonella Typhimurium and Enteritidis
isolated from different sources
|
Type of sample |
Salmonella
Typhimurium |
Salmonella Enteritidis |
Total |
|
|
Humans |
Hand swab |
7 |
2 |
9 |
|
Stool samples |
2 |
0 |
2 |
|
|
Food samples |
Chicken meat sample |
10 |
4 |
14 |
|
Egg samples |
7 |
9 |
16 |
|
|
Environmental samples |
Commercial broiler farms |
6 |
4 |
10 |
|
Transportation van samples |
13 |
6 |
19 |
|
|
Chopping board samples |
0 |
1 |
1 |
|
|
Total |
|
45 |
26 |
71 |
Table 2: Antimicrobial resistance (%) in Salmonella Typhimurium
isolated from different sources
|
Sample
Type (Typhimurium) |
No.
of isolates tested |
AMP |
AML |
S |
SF |
CIP |
C |
NA |
TE |
CN |
W |
|
Human
samples |
9 |
88.89 |
100 |
77.78 |
88.89 |
44.44 |
11.11 |
66.67 |
88.89 |
100 |
88.89 |
|
Food
samples |
17 |
23.53 |
94.12 |
76.47 |
35.29 |
29.41 |
29.41 |
64.71 |
100 |
76.47 |
88.24 |
%20263-269_files/image002.png)
Fig. 1: Resistance (%) of Salmonella Typhimurium
isolated from different sources against 10 antibiotics
resistance
of all S. Typhimurium serovars to 10
antimicrobial agents (Fig. 1).
Table 2
shows the antimicrobial resistance percentages of different antimicrobials
against S. Typhimurium isolated from human, food and environmental samples. All the strains (100%) were
resistant to at least one antimicrobial agent. The highest level of resistance
was found in amoxicillin (AML), gentamycin (CN), tetracycline (TE), and,
trimethoprim (W). All (100%) of human and environmental samples while (94.12%)
of food samples were resistant to AML. Similarly, (100%) of human and
environmental samples and (76.64%) were resistant to gentamycin (CN). The
higher level of resistance with (100%) of food samples, (94.74%) of
environmental samples and, (88.89%) of human samples were resistant to
tetracycline (TE). An equal level of high resistance was found (88%) in human
food and environmental samples. A moderate level of resistance was found
against AMP, SF, S, NA, C and CIP (in declining order) (Table 2).
A total of 25 resistance patterns were found (Table 3)
with the most common (16%) resistant pattern was (AMP, AML,
S, SF, C, NA, TE, CN, W). According to the patterns of antimicrobial
resistance, the highest resistance was shown in Salmonella Typhimurium
strains isolated from vehicles (13.33%) followed by chicken samples (28.8%),
human samples (20%), egg samples (15.5%) and (13.3%) in broiler farms samples. Four penta
MDR (ACSSuT) and two tetra MDR (ASSuT)
pattern were found is S. Typhimurium. (Table 3).
Fig. 2 showed the
resistance percentages of Salmonella Enteritidis isolated from different
sources against 10 antibiotics with the highest resistance found against sulphonamides and streptomycin. (Fig. 2).
A great proportion of antimicrobial resistance was found in Salmonella Enteritidis strains with
(96%) of the isolated strains showed resistance to at least one antimicrobial
agent (Table 4). The highest level of resistance was found in streptomycin (S),
tetracycline (TE), nalidixic acid (NA) and CN. All the human and environmental
(100%) samples while (92.31%) of food samples were resistant to streptomycin
(S). Similarly (100%) of human samples, (92.31%) of food samples and (91%) of
environmental samples were resistant to tetracycline (TE). Similarly, (100%) of
human and environmental Table 3: Antimicrobial resistance Patterns of Salmonella Typhimurium
|
Antibiotics
pattern |
Human
samples |
Chicken
samples |
Egg
samples |
Vehicle
samples |
Broiler
farm samples |
Total |
Percentage |
|
AMP,AML,S,CN |
0 |
0 |
0 |
0 |
1 |
1 |
2% |
|
AML,TE,CN,W |
0 |
0 |
1 |
0 |
0 |
1 |
2% |
|
AML,CIP,TE,W |
0 |
0 |
1 |
0 |
0 |
1 |
2% |
|
AML,S,SF,NA,TE, |
0 |
2 |
0 |
0 |
2 |
4% |
|
|
AML,S,TE,CN,W |
0 |
0 |
1 |
0 |
0 |
1 |
2% |
|
AML,S,SF,TE,CN,W |
0 |
1 |
1 |
0 |
0 |
2 |
4% |
|
AMP,AML,S,CIP,TE,W |
0 |
0 |
1 |
0 |
0 |
1 |
2% |
|
AMP,AML,S,NA,TE,CN |
1 |
0 |
0 |
0 |
0 |
1 |
2% |
|
AML,S,C,NA,TE,CN,W |
0 |
1 |
1 |
1 |
3 |
7% |
|
|
AMP,AML,C,NA,TE,CN,W |
0 |
0 |
0 |
1 |
0 |
1 |
2% |
|
AMP,AML,S,SF,NA,TE,CN |
0 |
1 |
0 |
0 |
0 |
1 |
2% |
|
AMP,AML,SF,NA,TE,CN,W |
1 |
0 |
0 |
0 |
0 |
1 |
2% |
|
AMP,AML,S,NA,TE,CN,W |
0 |
2 |
0 |
0 |
0 |
2 |
4% |
|
AMP,AML,S,SF,CIP,NA,TE,CN |
1 |
0 |
0 |
1 |
0 |
2 |
4% |
|
AMP,AML,SF,C,NA,TE,CN,W |
1 |
0 |
0 |
1 |
0 |
2 |
4% |
|
AML,S,CIP,C,NA,TE,CN,W |
0 |
1 |
0 |
0 |
0 |
1 |
2% |
|
AMP,AML,S,C,NA,TE,CN,W |
0 |
0 |
0 |
2 |
0 |
2 |
4% |
|
AML,S,SF,C,NA,TE,CN,W |
0 |
0 |
0 |
0 |
1 |
1 |
2% |
|
S,SF,CIP,C,NA,TE,CN,W |
0 |
0 |
0 |
0 |
0 |
0 |
0% |
|
AMP,AML,S,SF,NA,TE,CN,W |
1 |
1 |
0 |
0 |
1 |
3 |
7% |
|
AMP,AML,CIP,C,NA,TE,CN,W |
0 |
1 |
0 |
0 |
0 |
1 |
2% |
|
AML,S,SF,CIP,C,NA,TE,CN,W |
1 |
0 |
1 |
0 |
2 |
4 |
9% |
|
AMP,AML,S,SF,C,NA,TE,CN,W |
1 |
0 |
0 |
6 |
0 |
7 |
16% |
|
AMP,AML,S,SF,CIP,NA,TE,CN,W |
2 |
0 |
0 |
1 |
0 |
3 |
7% |
|
AMP,AML,S,SF,CIP,C,NA,TE, CN,W |
0 |
0 |
0 |
1 |
0 |
1 |
2% |
|
|
9 |
0 |
1 |
8 |
2 |
45 |
100% |
Table 4: Antimicrobial resistance (%) in Salmonella Enteritidis
isolated from different sources
|
Samples
(Enteritidis ) |
No.
of isolates tested |
AMP |
AML |
S |
SF |
CIP |
C |
NA |
TE |
CN |
W |
|
Human
samples |
2 |
50% |
50% |
100% |
50% |
50% |
50% |
100% |
100% |
100% |
50% |
|
Food
samples |
13 |
53.85 |
62% |
92.31 |
61.54 |
0% |
23.08 |
61.54 |
92.31 |
69.23 |
46.15 |
|
Environmental samples |
11 |
45% |
45% |
100% |
63.64 |
9.09 |
45% |
64% |
91% |
36% |
45% |
samples and (76.64%) were resistant to gentamicin
(CN). Again (100%) of human samples, (69.23%) and (61.54%) of food samples,
(36%) and (64%) of environmental samples were resistant to gentamicin (CN) and
nalidixic acid (NA) respectively. A moderate level of resistance was found
against AMP, AML, SF, W, C and CIP. (in declining
order) (Table 4). A total of 22 resistance patterns were
found for Salmonella Enteritidis with the most common pattern
among all samples were (S, NA, AML, W, TE, SF, AMP) which was 16% (Table 5). According to the patterns of antimicrobial resistance highest
resistance was shown in S. Enteritidis
strains isolated from egg samples (34.6%) followed by transportation van
samples (23.0%), chicken samples and broiler farms samples (15.3%), human
samples (7.6%) and least in chopping board samples (3.6%). Two penta
MDR (ACSSuT) and six tetra MDR (ASSuT)
resistance patterns were found in S. Enteritidis
(Table 5).
Discussion
In
developing countries of Asia including Pakistan antimicrobial drugs are
extensively used in food-producing animals and poultry for growth promotion and
prophylaxis. Food-borne bacteria can attain resistance as a result of extensive
use in food animals and can transmit these resistance genes to humans via the
food chain (Bouchrif et al. 2009). The importance of antimicrobial resistance
against zoonotic Salmonella serovar Enteritidis and Typhimurium has been shown in this study. In our study,
exponentially high resistance was found in Salmonella
Typhimurium isolates where all (100%)
of the strains isolated from different sources were resistant to at least one
antibiotic. One study from Minnesota reported (89%) of Salmonella Typhimurium
isolated from animals and (44%) from humans were resistant to at least one
antibiotic (Wedel et al. 2005). In two studies from Italy, one reported (75%)
of S. Typhimurium were resistant to
at least one antimicrobial agent (Busani et al. 2004), and the second
reported (87%) of human isolates and (81%) from animal source showed resistance
to at least one antibiotic (Graziani et al. 2008) The high level of
resistance found in our study may be due to widespread and over the counter use
of antimicrobials in humans and veterinary (poultry) medicine in Pakistan.
According to the source of
isolates a high level of resistance was found (76.64‒100%)
among isolates of humans, environmental and, food against amoxicillin (94‒100%),
gentamicin (76.64‒100%), tetracycline (88.89%) and trimethoprim (88%).
Moderate level of resistance was found against (in declining order) ampicillin
(45‒50%), sulphonamides (35‒88%),
Table 5: Anti Microbial Resistance
Patterns of Salmonella Enteritidis
|
AMR
Pattern |
Human
samples |
chicken
samples |
egg
samples |
transportation
van samples |
broiler
farm samples |
Chopping
board |
Total |
|
C,S |
0 |
0 |
1(11%) |
0 |
0 |
0 |
1(4%) |
|
S,TE |
0 |
1(25%) |
1(11%) |
0 |
0 |
0 |
2(8%) |
|
CN,S,TE |
0 |
0 |
0 |
0 |
1(25%) |
0 |
1(4%) |
|
S,NA,TE,AMP |
0 |
0 |
1(11%) |
0 |
0 |
0 |
1(4%) |
|
S,CIP,W,SF,C |
0 |
0 |
0 |
0 |
1(25%) |
0 |
1(4%) |
|
CN,S,TE,SF,AMP |
0 |
0 |
0 |
1(17%) |
0 |
0 |
1(4%) |
|
CN,NA,AML,W,TE |
0 |
1(25%) |
0 |
0 |
0 |
0 |
1(4%) |
|
CN,S,NA,AML,TE |
0 |
0 |
0 |
1(17%) |
0 |
0 |
1(4%) |
|
S,NA,TE,SF,AMP,C |
0 |
0 |
0 |
1(17%) |
0 |
0 |
1(4%) |
|
S,NA,W,TE,SF,C |
0 |
0 |
0 |
1(17%) |
0 |
0 |
1(4%) |
|
CN,S,NA,AML,TE,SF |
0 |
0 |
0 |
1(17%) |
0 |
0 |
1(4%) |
|
CN,S,CIP,NA,W,TE |
1(50%) |
0 |
0 |
0 |
0 |
0 |
1(4%) |
|
CN,S,NA,TE,SF,C |
0 |
1(25%) |
0 |
0 |
0 |
0 |
1(4%) |
|
CN,S,AML,W,TE,SF |
0 |
0 |
1(11%) |
0 |
0 |
0 |
1(4%) |
|
CN,S,NA,AML,TE,SF,AMP |
0 |
0 |
1(11%) |
0 |
0 |
0 |
1(4%) |
|
S,NA,AML,W,TE,SF,AMP |
0 |
0 |
1(11%) |
0 |
2(50%) |
1(100%) |
4(16%) |
|
S,NA,AML,W,TE,AMP,C |
0 |
0 |
0 |
1(17%) |
0 |
0 |
1(4%) |
|
S,NA,AML,W,TE,SF,C |
0 |
1(25%) |
0 |
0 |
0 |
0 |
1(4%) |
|
CN,S,AML,W,TE,SF,AMP |
0 |
0 |
1(11%) |
0 |
0 |
0 |
1(4%) |
|
CN,S,NA,AML,AMP,TE,SF,C |
1(50%) |
0 |
0 |
0 |
0 |
0 |
1(4%) |
|
CN,S,NA,AML,TE,SF,W,AMP |
0 |
0 |
1(11%) |
0 |
0 |
0 |
1(4%) |
|
S,NA,AML.W,TE,AMP,SF,CN |
0 |
0 |
1(11%) |
0 |
0 |
0 |
1(4%) |
|
|
2 |
4 |
9 |
6 |
4 |
1 |
26 |
%20263-269_files/image004.png)
Fig. 2: Resistance of Salmonella
Enteritidis isolated from different
sources
Streptomycin (76‒89%), nalidixic acid (64‒94%),
chloramphenicol (11‒73%) and ciprofloxacin (26‒44%). Our results are
inconsistent with reports from Italy that showed resistance to ampicillin
(67.6%), tetracycline (73.6%), streptomycin (65.4%), sulfonamides (73.3%) and
chloramphenicol (32.3%) (Graziani et al. 2008). Another study
reported from the UK showed (82%) of S.
Typhimurium were predominately
resistant to, sulfonamides, streptomycin, tetracycline’s, ampicillin, and
chloramphenicol, while (20%) were resistant to trimethoprim (Threlfall et al.
2003). Our results are also nearly equal to those reported from Italy,
showed (83.9%) of S. Typhimurium isolates showed resistance
to tetracycline, sulfamethoxazole, streptomycin, chloramphenicol and ampicillin
(De Vito et
al. 2015). Another study from Ireland reported (77.6%) of Typhimurium isolates were resistant to
ampicillin, chloramphenicol, streptomycin, sulfonamides and tetracycline (Gorman and Adley 2004). In the present study,
a very low level of resistance was found against ciprofloxacin as also reported
from Italy where all S. typhiurium isolates were susceptible to ciprofloxacin (Busani et al.
2004).
A total of 26 resistance patterns were found in Salmonella Typhimurium isolates of which 4 (ACSSuT)
and 2 (ASSuT) patterns were found. The highest
prevalent pattern was ((ASSuT) AML, NA, CN, W) which
was present in 16% of MDR Typhimurium
isolates. Our results are inconsistent with reports from China, Italy where the
most frequently observed patterns of resistance were (ACSSuT)
and (ASSuT) (Graziani et al. 2008; Wang et al. 2019).
A great proportion of antimicrobial resistance
was also found in S. Enteritidis
strains with, (96%) of the isolated strains showed resistance to at least one
antimicrobial agent. Maximum level (92.31%) of resistance was shown against sulphonamides and streptomycin and (69.23%) for nalidixic
acid. Our results are supported by a study in Brazil where (91%) of S. Enteritidis showed resistance to at
least one antimicrobial agent with the maximum level of resistance was found
against sulphonamides (75.8%) (Dias de Oliveira et al. 2005).
One study from Korea reported that (90%) of S.
Enteritidis strains were resistant to
sulphonamides and nalidixic acid (Hur et al.
2011) which is very close to our study. Another study from Taiwan
reported (70%) resistance to streptomycin and (75%) to tetracyclin
in two studies from Brazil reported (73.3%) and (28.12%) of S. enetritidis were resistant to nalidixic acid (Chu et al. 2009; Campioni
et al 2012; Campioni
et al. 2014). Nalidixic acid that
targets DNA gyrase is one of the common antimicrobials used for the treatment
of salmonellosis.
In the present study moderate level of resistance
was found against ampicillin (46.2%), amoxicillin (53.8%), gentamicin (50%),
trimethoprim (50%), tetracycline (50%), and chloramphenicol (50%). Lower level resistance was shown from a study in Brazil
where a low level of resistance was
found for tetracycline (15.4%), streptomycin (7.7%), gentamicin (5.5%),
trimethoprim (3.3%), ampicillin (1.1%), and chloramphenicol (1.1%). One study
from Iran in agreement with our study reported (100%) resistance of S. Enteritidis against ampicillin (70%)
against streptomycin and 60% against gentamicin(Ghazaey
and Mirmomeni 2012). The high level of resistance against different
antibiotics may be due to without prescription over the counter use in human
and veterinary medicine.
In the present study, a total of 22 resistance
patterns were found and the most prevalent pattern (16%) was ((ASSuT) W, AML, NA). A total of two (ACSSuT)
and four (ASSuT) were found in S.Enteritidis isolates. Our results are in agreement
with the study reported from Spain where 23 different resistant patterns were
found in S. Enteritidis (Carramiñana et
al. 2004).
Conclusion
An
alarmingly high level of resistance was found in both Salmonella Typhimurium
and Enteritidis isolated from humans,
food and environmental sample. In addition to this, our study isolates were
resistant to sulphonamides, nalidixic acid,
ampicillin, streptomycin and tetracycline is the indication of extensive use of
these antibiotics in human and veterinary medicine. In our study low level of
resistance and a high level of susceptibility were found against ciprofloxacin.
So fluoroquinolones can be the choice for treating
salmonellosis in our poultry industry.
Acknowledgments
Authors
acknowledge the poultry farmers and retail shop owners for provision of
samples. Authors are also thankful to the Laboratory staff of Department of
Epidemiology and Public Health for assistance in conduct of current study. The current research study was funded under
HEC Indigenous PhD program.
Author Contributions
MDA,
MC and HA planned the study, SS conduct the whole research work and MHM, JS and
SH help in formatting of manuscript.
Conflicts of Interest
Authors declare no conflict of
interest.
Data Availability
Data are available from the first author on reasonable request.
Ethics Approval
Not
applicable in this paper
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