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Advances in Infectious Diseases, 2021, 11, 49-59
https://www.scirp.org/journal/aid
ISSN Online: 2164-2656
ISSN Print: 2164-2648
DOI:
10.4236/aid.2021.111007 Mar. 11, 2021 49
Advances in Infectious Diseases
Occurrence of Multi-Drug Resistant Listeria
species in Faecal Samples of Poultry Chickens
in Rural Farms in Lagos State, Nigeria
Emelda E. Chukwu1*, Veronica N. Ibeh2, Olabisi F. Davies-Bolorunduro3
1Center for Infectious Diseases’ Research, Microbiology Department, Nigerian Institute of Medical Research, Yaba, Lagos State, Nigeria
2National Agency for Food and Drug Administration and Control, Lagos State, Nigeria
3Center for Tuberculosis Research, Microbiology Department, Nigerian Institute of Medical Research, Yaba, Lagos State, Nigeria
Abstract
Background:
Listeriosis is a common zoonotic disease caused by a foodborne
pathogen,
Listeria monocytogenes
. Poultry meat and products have been es-
tablished as vehicles of transmission of pathogenic
Listeria
strains to humans.
This study evaluates the occurrence of
Listeria species
in faeces
of poultry
chicken in Lagos.
Methods:
One hundred and fourteen pooled fresh faecal
samples from cage-re
ared broiler chickens were collected from 12 farms in
three rural areas in Lagos State from May to August 2019. All samples were
analysed for
Listeria
species detection according to ISO11290-
1 standard and
confirmed using PCR assay. Susceptibility testing
was performed using the
Kirby-Bauer disc diffusion technique.
Results:
Twenty-eight (24.6%)
Listeria
species were detected from 114 faecal samples. The isolated
Listeria
species
were
L. monocytogenes
8 (7.0%),
L. ivanovii
9 (7.9%),
L. grayi
7 (6.1%) and
L.
innocua
4 (3.5%). There was no significant difference in the frequency of oc-
currence of
Listeria
species across the different locations (X2 = 4.98, p =
0.08).
The listeria species were susceptible to Augmentin (96.4%),
vancomycin
(85.7%) and co-trimoxazole (82.1%), but resistant to ceftazidime (100%), te-
tracycline (75.0%) and ciprofloxacin (71.4%).
Conclusion:
This study reveals
high occurrence of multi-drug resistant
Listeria
species in faecal
samples of
poultry chickens in Lagos state which may be an important vector in the con-
tamination of the environment and transmission of antibiotic resistant
Li
s-
teria
species to consumers.
Keywords
Listeriosis,
Listeria monocytogenes
, Multi-Drug Resistance, Poultry Farms,
Zoonotic Disease, Chickens
How to cite this paper:
Chukwu,
E.E.,
Ibeh,
V.N. and Davies-Bolorunduro, O.F.
(20
21) Occurrence of Multi-
Drug Resistant
Listeria
species
in Faecal Samples of Poul-
try Chickens in Rural Farms in Lagos State,
Nigeria
.
Advances in Infectious Diseases
,
11
, 49-59.
https://doi.org/10.4236/aid.2021.111007
Received:
January 13, 2021
Accepted:
March 8, 2021
Published:
March 11, 2021
Copyright © 20
21 by author(s) and
Scientific
Research Publishing Inc.
This work is licensed under the Creative
Commons Attribution International
License (CC BY
4.0).
http://creativecommons.org/licenses/by/4.0/
Open Access
E. E. Chukwu et al.
DOI:
10.4236/aid.2021.111007 50
Advances in Infectious Diseases
1. Introduction
Listeria monocytogenes
infection is associated with consumption of food con-
taminated with animal faeces and has been reported as a common inhabitant of
the digestive tracts of animals including cattle, poultry and pigs [1]. Typical
sources of ingestion by humans are raw foods of animal and soil origin, such as
raw milk and dairy products, fresh meat, fruit, vegetables and seafood as well as
ready-to-eat (RTE) foods [1] [2] [3]
.
Reports of outbreaks have also followed in-
gestion of undercooked meat, poultry as well as coleslaw where it was first rec-
ognized as a food-borne zoonosis.
In Nigeria, poultry meat and products have been fingered as a potential vehi-
cle of transmission of pathogenic strains of Listeria to humans [4] [5] [6]. Early
studies on Listeria in Nigeria concentrated on the occurrence of the organism in
humans while studies on animals commenced in the late eighties. Occurrence of
the
L. monocytogenes
has been reported in farm animals in Nigeria. Ishola and
colleagues [5] reported high level (91.8%) of contamination of chicken flocks
and meat with
L. monocytogenes
in Oyo State, south-western Nigeria. An
outbreak of listeriosis was reported in a herd of cattle in the South-Western
city of Ibadan [7]. The organism was isolated in pure culture and the infected
animals were associated with still birth, abortion and nervous signs before death.
Chukwu
et al
. [8] reported the first case of
L. monocytogenes
infection in an Af-
rican buffalo (Syncerus caffer) that presented with septicaemia and abortion.
Although the animal recovered after treatment, the authors emphasized the need
for further investigation of listeriosis in wildlife. An early survey conducted by
Oni
et al
. [9] to determine the prevalence of antibody to Listeria serotypes in
1190 serum samples from various animal sources in Kano and Kaduna States
revealed that
L. monocytogenes
infection is widespread in domestic animals in
Nigeria.
Listeria species have been isolated from all stages of poultry production and
processing and emerging studies suggest that poultry birds might be an impor-
tant source of contamination of production processes which could lead to
transmission of infection to consumers [10]. This study therefore evaluates the
occurrence of
Listeria species
in faeces of poultry chicken in selected rural farms
in Lagos State, highlighting their antibiogram for further insight.
2. Methodology
Study Design/Sampling: The study was a cross-sectional survey of poultry
farms in rural areas in Lagos State. Three local government areas (Ikorodu, Epe
and Ojo) were purposively selected out of the four rural local government areas
(LGAs) in the state due to their accessibility. A list of all registered poultry farms
in each study location was constituted and used to randomly select four farms
per LGA using table of random numbers. Fresh faecal samples were collected
from cage-reared broiler chickens in 12 farms (4 farms per LGA) from May to
August 2019. The faecal samples were picked up early in the morning from each
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Advances in Infectious Diseases
site and pooled according to the cages (2 to 5 samples collected from different
areas representative of the cage). The samples were collected into sterile univer-
sal bottles and kept at refrigerator temperature until they reached the laboratory
for analysis as suggested by Hitchins
et al
. [11]. Microbiological and molecular
work was carried out at the Microbiology laboratory of the Nigerian Institute of
Medical Research.
Faecal culture:
This was done according to a modified version of the guideline stipulated by
standard ISO 11290-1. Faecal samples were pre-enriched in 9 ml of 0.1% pep-
tone water (1 part to 9 parts peptone water). The homogenized faecal material in
peptone water was incubated overnight at 35˚C. One ml of the homogenized
samples was transferred into 9ml of Listeria enrichment broth for selective en-
richment and incubated at 35˚C for 24 h as recommended by Curtis
et al
. [12].
Plating was done using the procedures of the Centre for Disease Control by us-
ing a sterile wire loop to inoculate the broth culture onto Listeria selective me-
dium agar base plates (Oxford formulation) and incubated at 35˚C for 24 hours
under anaerobic conditions. Typical colonies of
L. monocytogenes
were exam-
ined after 24 - 48 hours.
Identification and characterization of isolates
The Listeria isolates were presumptively identified on the basis of colonial
morphology and appearance, gram staining reaction, black halo production on
Listeria selective agar. They were subsequently inoculated into freshly pre-
pared Tryptose soy agar plate and used to carry out biochemical tests. Identi-
fication and classification of the different
Listeria
species were done using re-
sults of the biochemical tests including catalase test, motility test, and Christie,
Atkins, Munch-Petersen (CAMP) test as described by Rapeanu
et al
. [13],
β
-hemolytic activity and sugar fermentation tests (xylose, rhamnose, mannitol
and methyl d-mannopyranoside), oxidase test and methyl red voges proskauer
(MR-VP) tests as described by Dabrowski
et al
. [14]. All confirmed isolates
obtained were preserved in skimmed milk and Brain heart Infusion broth con-
taining 20% glycerol and stored at −80˚C.
Confirmation of Listeria species by molecular analysis: Polymerase Chain
Reaction
Bacteria DNA was extracted by Phenol Chloroform method [15] and the con-
centration of the DNA was quantified using nano drop spectrophotometer
(DeNovix DS-11 Spectrophotometer, Brazil) and read at 280 nm. The specific
detection of the
Listeria sp
ecies was based on PCR amplification of the 16S
rRNA gene using oligonucleotide primers [16]. Amplifications were carried out
using a final volume of 25 µL PCR super-mix comprising 12.5 μL Red Taq
Quick-Load 5× Master Mix with Standard Buffer (New England Biolabs, U.S.A.),
0.5 μL of each primer (10 μM), 4.5 μL of nuclease free water and 5 μL of bacterial
genomic DNA solution was subjected to thermocycling conditions (Eppendorf
master cycler gradient, Germany). The primers were
prs
Forward GCTGAA
GAGATTGCGAAAGAAG and Reverse CAAAGAAACCTTGGATTTGCGG.
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Cycling parameters included an initial denaturation step of 95˚C for 5 min, 35
cycles of a denaturation step of 95˚C for 30 s, a primer annealing step at 58˚C for
30 sec, an extension step at 72˚C for 45 s and final extension at 72˚C for 5 min.
The expected amplicon length for
Listeria species
was 370 bp. The PCR products
were separated using 1.5% agarose gel electrophoresis performed in an electro-
phoretic tank at 90 volts for 2.5 hours (Sigma Chemical Company), stained with
0.5 µg/ml ethidium bromide and photographed under UV transilluminator by
using a digital camera (Kodak Digital System DC-120). A DNA ladder digest of
100 bp was used as molecular weight marker.
Antimicrobial susceptibly testing
Antibiotic susceptibility assay to 12 commonly used antibiotics was performed
using the disk diffusion method (Kirby Bauer), according to the Clinical Labor-
atory Standards Institute criteria [17] on Mueller-Hinton agar plates (Oxoid,
UK). Inoculum suspension was prepared using sterile saline to obtain turbidity
comparable to 0.5 McFarland standards and sterile cotton swab was dipped, ro-
tated across the wall of the tube to avoid excess fluid and was evenly inoculated
on Muller-Hinton agar (Oxoid, UK). The antibiotic discs were placed on Mul-
ler-Hinton agar plates. The antibiotic discs that was used in this study were pe-
nicillin (10 µg), chloramphenicol (30 µg), Erythromycin (15 µg), ciprofloxacin (5
µg), gentamicin (10 µg), ofloxacin (5 µg), co-trimoxazole (25 µg), ceftazidime (30
µg), cefotaxime (30 µg), tetracycline (30 µg), vancomycin (30 µg) and augmentin
(30 µg). All the antibiotics were obtained from Oxoid laboratories (OXOID).
Lis-
teria monocytogenes
(ATCC 7644) and
E. coli
(ATCC 10536) were used as a
positive and negative control respectively. Diameters of the zones of inhibition
for individual antibacterial agents were translated into susceptible, intermediate,
and resistant categories, according to the clinical and laboratory standards insti-
tute criteria [17]. Multiple drug resistant microorganisms were defined as resis-
tant to three or more antibiotic classes.
Data analysis
Descriptive statistics were employed to obtain the frequencies and distribu-
tions. Nonparametric chi-squared tests were used to compare differences between
different rural areas. Data were analysed using SPSS version 26 (IBM, Chicago, IL).
P-value < 0.05 was considered statistically significant.
3. Results
Out of the 114 pooled fecal samples collected from the poultry, twenty-eight (28)
Listeria species were detected, giving an overall prevalence of 24.5% for listeria
species. All identified Listeria species showed bands at the 370 bp using Listeria
genus specific primer (Figure 1). The isolated Listeria species were
L. ivanovii
9
(7.9%),
L. monocytogenes
8 (7.0%),
L. grayi
7 (6.1%) and
L. innocua
4 (3.5%).
Epe had the highest prevalence 13/38 (34.1%) followed by Ikorodu 10/38
(26.3%) and Ojo 5/38 (13.1%) Table 1. However, there was no significant dif-
ference in the frequency of occurrence of Listeria species across the locations (X2
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Advances in Infectious Diseases
Figure 1. Agarose gel containing representative amplicon of Listeria species showing
bands at 370 bp using Listeria genus primer (PRS). Lane M, Molecular marker (100 bp
DNA ladder), Lane 1 negative control, Lane 2-positive control. Lanes 3 - 27 are repre-
sentative amplicon of Listeria species.
Table 1. Distribution of
Listeria species
among the different farms.
Rural
Farms
No of Feacal
samples
n = 114
No positive for
L.
monocytogenes
(%)
No positive for
L. ivanovii
(%)
No positive
for
L. grayi
(%)
No positive for
L. innocua
(%)
Total No
positive for
Listeria spp (%)
Ikorodu
38
5 (13.2)
3 (7.9)
1 (2.6)
1 (2.6)
10 (26.3)
Ojo
38
1 (2.6)
1 (2.6)
1 (2.6)
2 (5.3)
5(13.1)
Epe
38
2 (5.3)
5 (13.1)
5 (13.1)
1 (2.6)
13 (34.1)
Total
114
8(7.0%)
9(7.9%)
7(6.1%)
4(3.5%)
28 (24.5)
Table 2. Antibiotic susceptibility pattern of Listeria species Isolated.
ANTIBIOTICS
SUSCEPTIBLE
(%)
N = 28
INTERMEDIATE
(%)
N = 28
RESISTANCE
(%)
N = 28
VANCOMYCIN
24 (85.7)
0 (0)
4 (14.3)
ERYTHROMYCIN
7 (25.0)
7 (25,0)
14 (50.0)
CHLORAMPHENICOL
20 (71.4)
2 (7.1)
6 (21.4)
TETRACYCLINE
7 (25.0)
0 (0)
21 (75.0)
CEFTAZIDIME
0 (0)
0 (0)
28(100)
CEFOTAXIME
1 (3.6)
3(10.7)
24 (85.7)
GENTAMICIN
12 (42.9)
2 (7.1)
14 (50.0)
CIPROFLOXACIN
8 (28.6)
0 (0)
20 (71.4)
OFLOXACIN
8 (28.6)
0 (0)
20 (71.4)
AMOXYCILLIN/CLAVULANATE
27 (96.4)
0 (0)
1 (3.6)
PENICILLIN G
20 (71.4)
6 (21.4)
2 (7.1)
CO-TRIMOXAZOLE
23 (82.1)
4 (14.3)
1 (3.6)
= 4.98, p = 0.08).
Listeria monocytogenes
prevalence of 7.0% was recorded in
this study.
Listeria species isolated showed a high level of resistance to the tested anti-
biotics (Table 2). In general, the listeria species were susceptible to Augmentin
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Advances in Infectious Diseases
Figure 2. Antibiotic susceptibility pattern of
Listeria monocytogen
Isolates.
(96.4%), vancomycin (85.7%), co-trimoxazole (82.1%), penicillin G (71.4%) and
chloramphenicol (71.1%) but resistant to ceftazidime (100%), cefotaxime (85.7%),
tetracycline (75.0%), ciprofloxacin (71.4%), ofloxacin (71.4%), gentamicin (50%)
and erythromycin (50%). The study recorded very low susceptibility to the qui-
nolones tested (ciprofloxacin and ofloxacin). A large proportion of the Listeria
isolates (22/28 (78.6%)) were resistant to 3 or more classes of antibiotics with an
average resistance of 4.6 antibiotics classes. Similarly, the
Listeria monocytogenes
strains were resistant to ceftazidime (100%), cefuroxime (100%), ciprofloxacin
(87.5%), tetracycline (87.5%), ofloxacin (75.0%), erythromycin (75%) and genta-
mycin (62.5%) Figure 2.
4. Discussion
Poultry farming is a common practice in Nigeria, especially in rural areas. Many
people raise poultry in large or small scale within their homes and these birds are
used to produce eggs or meat, while the manure is used as a supplement or subs-
titute for inorganic fertilizers on Nigerian farms. Four major Listeria species in-
cluding
Listeria ivanovii
,
L. monocytogenes
,
L. grayi
and
L.innocua
were identi-
fied from rural farms in Lagos State. These key listeria species have also been
reported by previous studies as major contaminants of foods sold in different
parts of Nigeria [6] [18] [19] [20]. Daniel
et al
. [4], reported 14.17% contamina-
tion rate for listeria species in commercially frozen and fresh chicken sold within
Markurdi metropolis, Nigeria with
L. grayi
(58.82%) standing out as the most
occurring species.
Listeria monocytogenes
cause a rare but often severe illness known as Listeri-
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osis which is most often characterized by febrile gastroenteritis, sepsis, and me-
ningitis and may result in severe illness or death especially in immunocompro-
mised individuals [21]. The low prevalence of
L. monocytogenes
(7.0%) record-
ed in this study agrees with a study in France where 10.5% contamination of feacal
samples of laying and broiler flocks with
L. monocytogenes
was reported [10].
However, the findings contrast with a previous study in Oyo State South-Western
Nigeria which reported high level (91.5%) of contamination of chicken flocks and
meat with
L. monocytogenes
[5]. Comparison of prevalence results among dif-
ferent studies can be influenced by variation in sampling strategies and differ-
ences in detection methods used. A study in Sokoto Nigeria [22] detected Lis-
teria in 39 out of 192 raw milk samples collected from lactating cows in nomadic
herds and small-scale dairy farms. The implicated
Listeria
species were
innocua
,
L. ivanovii
,
L. monocytogenes
,
L. welshimeri
and
L. selegeri
and the authors al-
luded it to environmental contamination due to unhygienic milking. Another
report identified poor methods of pasteurization as a major contributor to high
microbial counts in milk [23].
The overall prevalence of listeria species (24.5%) and
Listeria monocytogenes
(7.0%) recorded in our study unveils potential faecal shedding of
Listeria species
in poultry chicken in rural farms in Lagos State and this could be a likely source
of environmental contamination and could ultimately result in transmission of
multi-drug resistant Listeria infections to humans. This finding is coming at
heels of a recent report of an alarming low level of knowledge of food-borne ill-
ness caused by
L. monocytogenes
among pregnant women attending a tertiary
healthcare center in Lagos Stats, albeit pregnant women are globally adjudged to
be at increased risk of acquiring listeriosis [24]. A study in France investigated
774 poultry samples and concluded that
L. monocytogenes
is prevalent in the
production systems of laying hens (15.5%) and broilers (32%) [10].
The
Listeria
species isolated in this study showed a high level of resistance to
the tested antibiotics with majority (78.6%) of the Listeria isolates resistant to 3
or more classes of antibiotics (Multi-drug resistance). Similar resistance trends
have been reported in listeria species isolated from frozen meat [6], chicken and
chicken flocks [4] [5] as well as ready-to-eat vegetables and raw milk sold across
Nigeria. Studies have observed a pattern of emergence of resistance among strains
of
Listeria
spp isolated from food and domestic animals which are resistant to one
or more antibiotics [25] [26]. Although
Listeria
species showed moderate suscep-
tibility to penicillin which is the drug of choice in the treatment of Listeriosis,
resistant to quinolones which are wide spectrum antibiotics used in the treat-
ment of most bacterial infection is a cause for concern.
Listeria
species can either
acquire or transfer antibiotic resistances’ genes from plasmid and transposons of
other bacterial species either
in vivo
or
in vitro
in the intestinal tract [27]. A re-
cent study by Omogbai and Esokpunwu [6] similarly revealed emerging resis-
tancein
Listeria
species isolated, with most resistant to Ampiclox, Amoxicillin
and Septrin.
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Listeria monocytogenes
species isolated in this study exhibited high level of an-
tibiotic resistance as well. This is worrisome because Listeriosis caused by
L. mo-
nocytogenes
can have mortality rates as high as 30%, especially among vulnerable
groups such as infants, pregnant women and the elderly even without being re-
sistant [28]. Therefore, development of antimicrobial resistance by this group of
bacteria could portend a huge public health and economic burden. As a proac-
tive measure, most western countries have taken the initiative to develop policies
and guidelines to monitor and control
L. monocytogenes
in foods as well as
educate vulnerable population on the need to avoid high risk foods. Unfortu-
nately, such interventions do not exist in Nigeria and some other African coun-
tries. Resistance to the cephalosporins (Ceftazidime 100% and Cefuroxime
100%) recorded in this study is not surprising as
Listeria monocytogenes
strains
have been shown to be intrinsically resistant to broad spectrum cephalosporins
[29]. However, resistant to flouroquinolones (ciprofloxacin 87.5% and ofloxacin
75.0%) which are broad spectrum antibiotics recorded in this study is a cause for
concern and may be attributable to the indiscriminate use and abuse in human
and veterinary medicine. The choice drug for treating listeriosis is a
β
-lactam (am-
picillin or penicillin) alone or combined with an aminoglycoside usually gentami-
cin [30]. However, the
L. monocytogenes
strains were moderately susceptible to
Augmentin (75.0%) and Gentamicin (62.5%). This finding supports a previous
study by Ishola
et al
. [5] who reported 100% resistance to cefuroxime by the
L.
monocytogenes
isolated from chicken and chicken flocks tested while the high-
est sensitivity (86.1%) was obtained with amoxicillin clavulanate. In a study on
human
Listeria monocytogenes
strains in Brazil, all strains were susceptible to
ampicillin, cephalothin, erythromycin, gentamicin, teicoplanin and vancomycin
[31] while only one (1.5%), and two (3%) strains showed resistance to rifampin
and trimethoprim-sulfamethoxazole respectively [31]. The growing trend of an-
tibiotic resistance among Listeria species may be attributable to indiscriminate
use of antibiotics in poultry farming as growth promoters and for treatment of
infections [32]. In light of the recent zoonotic outbreak and shift towards a one
health paradigm. There is need to urgently address the emergence of resistance
through implementation of antibiotic stewardship in veterinary science as well
as establish a monitoring trend for the development of antimicrobial resistance
among this organism.
One major limitation of the study is that the LGAs were purposively selected
and may not be a true representative of the entire rural community in Lagos
State. Also, the low sample size used in this study prevents generalization of
findings. A further research into the genetic variations of listeria species with
reference to resistance/susceptibility to common antibiotics using a larger sam-
ple is required for better understanding of the epidemiological trend.
5. Conclusion
There was a high occurrence of multi-drug resistant Listeria species in faecal
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Advances in Infectious Diseases
sample of poultry chickens in Lagos state which may be an important vector in
the contamination of the environment and transmission of antimicrobial resis-
tant
Listeria
to consumers. Our findings suggest that poultry chicken may rep-
resent a potentially important reservoir for multi-drug resistant Listeria species.
This underscores the need for implementation of proper hygienic and sanitary
measures during slaughtering and evisceration operations to prevent zoonotic
transmission of Listeria species through consumption of contaminated chicken
meat and eggs by humans.
Author’s Contribution
This work was done in collaboration among all authors. The first author EEC
designed the study, wrote the draft manuscript and corresponded with the jour-
nal. Authors EEC, VNI and OFD participated in the sample collection and labo-
ratory analysis. Author EEC conducted the data analysis. All authors contributed
to the literature searches and approved the final manuscript.
Conflicts of Interest
The authors declare no conflicts of interest regarding the publication of this
paper.
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