Diversity of bacterial pathogens and their antimicrobial resistance profile among commensal rodents in Qatar

Abstract

Rodents are sources of many zoonotic pathogens that are of public health concern. This study investigated bacterial pathogens and assessed their antimicrobial resistance (AMR) patterns in commensal rodents in Qatar. A total of 148 rodents were captured between August 2019 and February 2020, and blood, ectoparasites, and visceral samples were collected. Gram-negative bacteria were isolated from the intestines, and blood plasma samples were used to detect antibodies against Brucella spp., Chlamydophila abortus, and Coxiella burnetii. PCR assays were performed to detect C. burnetii, Leptospira spp., Rickett-sia spp., and Yersinia pestis in rodent tissues and ectoparasite samples. Antimicrobial resistance by the isolated intestinal bacteria was performed using an automated VITEK analyzer. A total of 13 bacterial species were isolated from the intestine samples, namely Acinetobacter baumannii, Aeromonas salmonicida, Citrobacter freundii, Citrobacter koseri, Enterobacter aerogenes, Enterobacter cloacae, Escherichia coli, Hafnia alvei, Klebsiella pneumoniae, Providencia stuartii, Proteus mirabilis, Pseudomonas aeruginosa, and Salmonella enterica. The majority of them were E. coli (54.63%), followed by P. mirabilis (17.59%) and K. pneumoniae (8.33%). Most of the pathogens were isolated from rodents obtained from livestock farms (50.46%), followed by agricultural farms (26.61%) and other sources (22.94%). No antibodies (0/148) were detected against Brucella spp., C. abortus, or C. burnetii. In addition, 31.58% (6/19) of the flea pools and one (1/1) mite pool was positive for Rickettsia spp., and no sample was positive for C. burnetii, Leptospira spp., and Y. pestis by PCR. A total of 43 (38%) bacterial isolates were identified as multidrug resistant (MDR), whereas A. salmonicida (n = 1) did not show resistance to any tested antimicrobials. Over 50% of bacterial MDR isolates were resistant to ampicillin, cefalotin, doxycycline, nitrofurantoin, and tetracycline. The presence of MDR pathogens was not correlated with rodent species or the location of rodent trapping. Seven (11.86%) E. coli and 2 (22.2%) K. pneumoniae were extended-spectrum beta-lactamases (ESBL) producers. These findings suggest that rodents can be a source of opportunistic bacteria for human and animal transmission in Qatar. Further studies are needed for the molecular characterization of the identified bacteria in this study.

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Veterinary Research Communications
https://doi.org/10.1007/s11259-021-09876-2
ORIGINAL ARTICLE
Diversity ofbacterial pathogens andtheir antimicrobial resistance
profile amongcommensal rodents inQatar
MdMazharulIslam1,2 · ElmoubasharFarag3· MohammadMahmudulHassan4 · KhalidA.Enan1,5·
K.V.MohammadSabeel1· MaryamMohammedAlhaddad1· MariaK.Smatti6· AbdullaMohammadAl‑Marri1·
AbdulAziaAl‑Zeyara1· HamadAl‑Romaihi3· HadiM.Yassine6· AliA.Sultan7· DevendraBansal3·
ZilungileMkhize‑Kwitshana2,8
Received: 21 June 2021 / Accepted: 12 December 2021
© Springer Nature B.V. 2022
Abstract
Rodents are sources of many zoonotic pathogens that are of public health concern. This study investigated bacterial pathogens
and assessed their antimicrobial resistance (AMR) patterns in commensal rodents in Qatar. A total of 148 rodents were cap-
tured between August 2019 and February 2020, and blood, ectoparasites, and visceral samples were collected. Gram-negative
bacteria were isolated from the intestines, and blood plasma samples were used to detect antibodies against Brucella spp.,
Chlamydophila abortus, andCoxiella burnetii. PCR assays were performed to detect C. burnetii, Leptospira spp., Rickett-
sia spp., and Yersinia pestis in rodent tissues and ectoparasite samples. Antimicrobial resistance by the isolated intestinal
bacteria was performed using an automated VITEK analyzer. A total of 13 bacterial species were isolated from the intestine
samples, namely Acinetobacter baumannii, Aeromonas salmonicida, Citrobacter freundii, Citrobacter koseri, Enterobacter
aerogenes, Enterobacter cloacae, Escherichia coli, Hafnia alvei, Klebsiella pneumoniae, Providencia stuartii, Proteus
mirabilis, Pseudomonas aeruginosa, and Salmonella enterica. The majority of them were E. coli (54.63%), followed by P.
mirabilis (17.59%) and K. pneumoniae (8.33%). Most of the pathogens were isolated from rodents obtained from livestock
farms (50.46%), followed by agricultural farms (26.61%) and other sources (22.94%). No antibodies (0/148) were detected
against Brucella spp., C. abortus, or C. burnetii. In addition, 31.58% (6/19) of the flea pools and one (1/1) mite pool was
positive for Rickettsia spp., and no sample was positive for C. burnetii, Leptospira spp., and Y. pestis by PCR. A total of 43
(38%) bacterial isolates were identified as multidrug resistant (MDR), whereas A. salmonicida (n = 1) did not show resist-
ance to any tested antimicrobials. Over 50% of bacterial MDR isolates were resistant to ampicillin, cefalotin, doxycycline,
nitrofurantoin, and tetracycline. The presence of MDR pathogens was not correlated with rodent species or the location of
rodent trapping. Seven (11.86%) E. coli and 2 (22.2%) K. pneumoniae were extended-spectrum beta-lactamases (ESBL)
producers. These findings suggest that rodents can be a source of opportunistic bacteria for human and animal transmission
in Qatar. Further studies are needed for the molecular characterization of the identified bacteria in this study.
Keywords Commensal rodents· Gram-negative bacteria· Rickettsia· Antimicrobial resistance· Qatar
Introduction
The global importance of emerging and reemerging infec-
tious diseases has increased immensely in the last few dec-
ades, with over 60% of them are of zoonotic origin (Jones
etal. 2008; Mostafavi etal. 2021). Rodents are poten-
tial sources of more than 88 zoonotic pathogens and are
historically linked to multiple epidemics (Bessat 2015;
Hashemi Shahraki etal. 2016; Islam etal. 2021a; Rosenthal
and Michaeli 1977). Commensal rodents, that live close to
humans and share human food, water, and shelter for liv-
ing, are common causes of damage to crops, destruction of
resources, and disease transmission (Meerburg etal. 2009;
Pinto 1993; Rabiee etal. 2018). Typical pathways for patho-
gen transmission from rodents to humans by direct contact;
food and water contaminated with rodent urine, feces, or
fur; or through their ectoparasites and other animals, such as
livestock and pets (Hamidi 2018; Rabiee etal. 2018).
* Md Mazharul Islam
mmmohammed@mme.gov.qa
Extended author information available on the last page of the article

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Qatar is a small country located in the Arabian Penin-
sula (World Travel Guide 2019) with a diverse population
(Planning and Statistics Authority 2020). Recently, three
commensal rodent species have been reported in Qatar: Mus
musculus, Rattus norvegicus, and Rattus rattus (Islam etal.
2021b; Noureldin and Farrag 2010). The cestode, Hyme-
nolepis diminuta, was found in R. norvegicus (Abu-Madi
etal. 2005), which is of public health importance (Torger-
son and Macpherson 2011). Several rodent-borne bacterial
diseases, such as campylobacteriosis (Abu-Madi etal. 2016;
Ghunaim etal. 2015; Humphrey etal. 2016; Mohammed
etal. 2015), non-diphtheritic corynobacteriosis (El-Nemr
etal. 2019), Escherichia coli enteritis (Ghunaim etal. 2015;
Humphrey etal. 2016; Mohammed etal. 2015), listeriosis
(Khan etal. 2017), Q-fever (Royal etal. 2013), salmonellosis
(Ghunaim etal. 2015; Humphrey etal. 2016), tuberculosis
(Al Marri 2012), and non-plague yersiniosis (Ghunaim etal.
2015) have been reported in humans and animals in Qatar.
Q-fever, brucellosis, and chlamydiosis are major causes of
livestock abortion in Qatar (Department of Animal Resource
2019).
The majority of Qatari residents originate from the
Indian subcontinent, which is endemic for many rodent-
borne zoonotic diseases, such as typhoid fever (Centers
for Disease Control and Prevention 2020; World Health
Organization 2018). Hence, frequent travel between Qatar
and these countries poses a risk of transboundary transmis-
sion of rodent-borne diseases in Qatar (Islam etal. 2021a;
Mangili and Gendreau 2005). Qatar has antimicrobial stew-
ardship programs (ASPs) in the medical field (Helen etal.
2018), although no legislation and guidelines are available
for its use in the veterinary field. Several studies have been
performed to determine the antimicrobial sensitivity (AST)
and Antimicrobial resistance (AMR) profiles of bacterial
isolates from humans and animals (Alhababi etal. 2020;
Sid Ahmed etal. 2020). Previous reports showed that urban
rodents could be potential carriers of AMR bacteria (Gwenzi
etal. 2021; Huy etal. 2020). However, presently there is
insufficient scientific data on the zoonotic bacteriaand their
AMR profile from wildlife, such as rodents in Qatar. There-
fore, this study investigated the diversity of rodent-borne
bacterial pathogens and their AMR patterns to assess the
public health risk in Qatar.
Methods
The sample collection
A total of 148 rodents were captured between August
2019 and February 2020 from different municipalities
and environments (Fig.1). A detail of these rodents was
described previously (Islam etal. 2021b). They included
three commensal species; M. musculus (n = 4), R. norvegi-
cus (n = 86), and R. rattus (n = 18). After administering
general anesthesia using 5% isoflurane inhalation (Mar-
quardt etal. 2018), cardiac blood was collected (Parasura-
man etal. 2010), and fleas and mites were captured from
rodents skin (Herrero-Cófreces etal. 2021; Stekolnikov etal.
2019). In addition, 108 rodents were necropsied, and six
visceral samples were collected from each rodent, includ-
ing the diaphragm, intestine, kidney, liver, lung, and spleen.
Information related to each rodent, such as species, age, sex,
pregnancy, ectoparasite type, ecosystem facility, and munici-
pality, was recorded.
Isolation, identification, andantimicrobial
resistance testing
All rodent intestines were processed under a laminar
airflow cabinet with a BSL 2 facility (Labconco, Cat:
3620924, Sl: 060757988) for the gram-negative gut bac-
terial isolation. Using sterilized swabs, the intestinal
contents were inoculated on MacConkey agar (MCA),
Hektoen enteric agar (HEA), eosin methylene blue agar
(EMBA), and selenite cystine broth (SCB) and incubated
overnight at 37°C. Growth on SCB was subcultured on
MCA, HEA, and EMBA. The colony characteristics were
studied on each culture medium, and the isolates were
primarily identified (Vandepitte 2003; Washington etal.
1985). Subsequent sub-cultures from the MCA, HEA,
and EMBA were performed to obtain a single colony. An
identical single colony of each primarily identified bacte-
rial species from a single rodent sample was transferred to
the automated VITEK system (VITEK®2, Version 07.01
compact system, Ref: 27630, SL: VK2C9944) for con-
firmatory identification and AST following the VITEK
protocol (VITEK 2008). A gram-negative identification
kit (VITEK® 2 GN kit, Ref: 21341) was used to confirm
the identification of the isolates. The minimum inhibi-
tory concentration (MIC) of an antimicrobial is the lowest
concentration of the antimicrobial that inhibits the growth
of a microorganism after overnight incubation (Andrews
2001). Using MIC, we checked the antimicrobial resist-
ance of the isolates using two cards: VITEK® 2 AST-GN
38 for samples number 1–65, and because of the produc-
tion of AST-GN 38 being halted by the manufacturer,
we alternated to VITEK® 2 AST-GN 85 for the rest of
the samples (samples number 66–108). These two cards
tested AMR against 20 antimicrobials: amikacin, amoxi-
cillin/clavulanic acid, ampicillin, cefalotin, cefovecin,
cefpodoxime, ceftiofur, chloramphenicol, doxycycline,
enrofloxacin, gentamicin, imipenem, marbofloxacin,
neomycin, nitrofurantoin, piperacillin, pradofloxacin,
tetracycline, tobramycin, trimethoprim/sulfamethoxazole.

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If an isolate was resistant to three or more antimicrobi-
als, it was considered MDR (Magiorakos etal. 2012).
The VITEK 2 AST-GN cards also tested the extended-
spectrum beta-lactamase (ESBL) producing ability of the
isolated E. coli and Klebsiella pneumoniae.
ELISA
Antibodies against Brucella spp., Chlamydophila abor-
tus, and Coxiella burnetii were quantified in plasma by
indirect IgG ELISA kits (IDVet, 310 rue Louis Pasteur
– 34,790 Grabels, France), following the manufacturer’s
protocol.
Fig. 1 Location of the different
municipalities of Qatar and
the facilities for trapping of
commensal rodents for isolating
bacterial pathogens in the cur-
rent study

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Molecular assays
Sample processing andDNA extraction
Genomic DNA was extracted from homogenized materials
of rodent tissues and ectoparasite samples using DNeasy
DNA blood and tissue (QIAGEN GmbH, Germany) as
per the manufacturer’s instructions. The visceral samples
of each rodent were grouped as a single tissue pool. The
fleas (n = 250) were collected into 19 pools (9–25 fleas per
pool) based on the flea sex and origin of the rodent host. All
mites (n = 4) were combined as a single pool. The tissue and
ectoparasite pools were homogenized in a 2ml microtube
(Sarstedt, 72.694.006) using a speed mill for two minutes
with 1mm, 4mm, and 30mm ceramic beads in 500μL
DMEM, 5% Gln, 1% Penstrep, 3% FKS. The microtube was
centrifuged for five minutes at 13000rpm, and the superna-
tant was transferred to a new 1.5ml tube and centrifuged at
13000rpm for 15min.
Molecular detection ofbacteria
Real-time PCR was carried out to detect DNA of Leptospira
spp., Rickettsia spp., and Yersinia pestis using 2X master
mix (5x Hot FIREPol Probe Universal qPCR Mix, Solis
BioDyne, Estonia) by Gentier 96E Real-time PCR System
(Tianlong Science and Technology, China). Conventional
PCR using AddStart Taq Master (2X concentration, South
Korea) was used to identify genomic DNA of C. burnetii
by SimpliAmp Thermal cycler and GDS-200C Gel docu-
mentation system. The PCR reaction conditions and primer/
probe used are listed in Table1. The positive DNA of C.
burnetii was used from our internal positive control stock
in the Department of Animal Resources, Qatar. However,
positive DNA of Rickettsia spp., Listeria spp., and Y. pestis
was collected from the Central Laboratory of the Ministry of
Higher Education and Scientific Research, Sudan. Distilled
water was used as the negative control.
Data analysis
All analyses were performed using the STATA/IC-13
(STATA Corp LLC, Lakeway Drive, TX, USA). Descriptive
statistics were expressed as frequency number, percentage
(%), and 95% confidence intervals (CI). The relationship
between bacterial isolation and MDR isolates with rodent
species and trapping locations were analyzed. The p value
(<0.05) was considered as a significant variation among the
variables.
Table 1 Primers, probes, and the annealing temperature for detecting Leptospira spp. and Rickettsia spp. used in rodent and ectoparasite samples
the current study
Pathogen and sample Primer name Primer (5′-3′) Annealing temperature Reference
Coxiella burnetii; Tissue
and flea
C. burnetii(F) CGG GTT AAG CGT GCT CAG TAT GTA 95°C for 10min,
35cycles of 95°C
20s, 60°C for 30s,
72°C for 45s, and
72°C for 5min
(Bruin etal. 2011)
C. burnetii(R) TGC CAC CGC TTT TAA TTC CTC CTC
Leptospira spp.; Tissue LipL32(F) AGA GGT CTT TAC AGA ATT TCT
TTC ACT ACCT
50°C for 2min, 95°C
for 10min, 40cycles
of 95°C for 15s,
60°C for 1min
(Tellevik etal. 2014)
LipL32(R) TGG GAA AAG CAG ACC AAC AGA
LipL32 (Probe) FAM-AAG TGA AAG GAT CTT TCG T
TGC-MGB
Rickettsia spp.; Tissue flea,
and mite
PanR8(F) AGC TTG CTT TTG GAT CAT TTGG 94°C for 2min,
45cycles of 94°C
for 15s, 60°C for
30s
(Kato etal. 2013)
PanR8(R) TTC CTT GCC TTT TCA TAC ATCTA
GT
PanR8(Probe) FAM-CCT GCT TCT ATT TGT CTT GC
AGT AAC ACG CCA -BHQ1
Yersinia pestis; Tissue and
flea
Yp-F132(F) CTG CAA GCA CCA CTG CAA C 95°C for 10min,
35cycles of 95°C
20s, 60°C for 30s,
72°C for 45s, and
72°C for 5min
(Hinnebusch and
Schwan 1993)
Yp-R560(R) TAC GGT TAC GGT TAC AGC ATC AGT G

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Results
Demography ofidentified bacteria
Among the 108 rodent intestine samples, 95 (87.95%,
95%CI: 80.30–93.43) were positive for gram-negative bac-
teria. Of these, 14.74% (n = 13, 95%CI: 8.30–23.49) of the
rodents carried two or more bacterial species. Most of the
positive rodents were collected from livestock farms (n = 54,
50.46%, 95%CI: 40.72–60.18), followed by agricultural
farms (n = 30, 26.61%, 95%CI: 18.60–35.93) and other
areas (n = 26, 22.94%, 95%CI: 15.43–31.97). The study
detected 110 isolates from 13 bacterial species (Table2).
The majority of the isolates were E. coli (54.763%, 95%CI:
44.76–64.24), followed by Proteus mirabilis (17.59%,
95%CI: 10.94–26.10), and Klebsiella pneumoniae (8.33%,
95%CI: 3.88–15.23).
Furthermore, E. coli were found to be prevalent in all
species of rodents: M. musculus (100%), R. norvegi-
cus (54.12%), and R. rattus (47.37%) (Table3). On the
other hand, P. mirabilis was detected only in R. norvegi-
cus (20.00%) and R. rattus (10.53%). The majority of E.
coli were isolated from the rodents of agricultural farms
(61.54%), followed by the livestock farms (53.33%), and
Table 2 Overall prevalence of rodent intestinal gram-negative bacte-
ria from Qatar
Bacteria Total number of iso-
lates, % (95% CI)
Family: Moraxellaceae
Acinetobacter baumannii 2, 1.85 (0.22–6.53)
Family: Aeromonadaceae
Aeromonas salmonicida 1, 0.93 (0.02–5.05)
Family: Enterobacteriaceae
Citrobacter freundii 2, 1.85 (0.22–6.53)
Citrobacter koseri 2, 1.85 (0.22–6.53)
Enterobacter aerogenes 3, 2.73 (0.58–7.90)
Enterobacter cloacae 3, 2.73 (0.58–7.90)
Escherichia coli 59, 54.63 (44.76–64.24)
Klebsiella pneumoniae 9, 8.33 (3.88–15.23)
Salmonella enterica 3, 2.73 (0.58–7.90)
Family: Hafniaceae
Hafnia alvei 1, 0.93 (0.02–5.05)
Family: Morganellaceae
Proteus mirabilis 19, 17.59 (10.94–26.10)
Providencia stuartii 2, 1.85 (0.22–6.53)
Family: Pseudomonadaceae
Pseudomonas aeruginosa 4, 3.70 (1.02–9.21)
Table 3 Univariate association of rodent intestinal gram-negative bacteria with rodent host species and trapping location in Qatar
*p < 0.05 was considered as significant variation among the variables
Bacteria (N = 110) Species wise positive; n (%) Trapping location wise positive; n (%)
Mus musculus
(n = 4)
Rattus
norvegicus
(n = 91)
Rattus rattus
(n = 15)
p
value*
Agricultural
farm (n = 30)
Livestock
farm
(n = 54)
Other areas
(n = 26)
p
value*
Acinetobacter
baumannii 0 (0.00) 1 (1.18) 1 (5.26) 0.47 0 (0.00) 0 (0.00) 2 (9.09) 0.02
Aeromonas salmo-
nicida 0 (0.00) 0 (0.00) 1 (5.26) 0.09 0 (0.00) 1 (1.67) 0 (0.00) 0.67
Citrobacter fre-
undii 0 (0.00) 2 (2.35) 0 (0.00) 0.76 1 (3.85) 1 (1.67) 0 (0.00) 0.61
Citrobacter koseri 0 (0.00) 0 (0.00) 2 (10.53) 0.01 0 (0.00) 1 (1.67) 1 (1.85) 0.50
Enterobacter
aerogenes 0 (0.00) 3 (3.53) 0 (0.00) 0.66 2 (7.69) 1 (1.67) 0 (0.00) 0.20
Enterobacter
cloacae 0 (0.00) 3 (3.53) 0 (0.00) 0.66 0 (0.00) 2 (3.33) 1 (4.55) 0.59
Escherichia coli 4 (100.00) 46 (54.12) 9 (47.37) 0.15 16 (61.54) 32 (53.33) 11 (50.00) 0.69
Hafnia alvei 0 (0.00) 1 (1.18) 0 (0.00) 0.87 0 (0.00) 0 (0.00) 1 (4.55) 0.14
Klebsiella pneu-
moniae 0 (0.00) 9 (10.59) 0 (0.00) 0.27 2 (7.69) 5 (8.33) 2 (9.09) 0.99
Providencia
stuartii 0 (0.00) 2 (2.35) 0 (0.00) 0.76 1 (3.85) 0 (0.00) 1 (4.55) 0.28
Proteus mirabilis 0 (0.00) 17 (20.00) 2 (10.53) 0.40 6 (23.08) 9 (15.00) 4 (18.18) 0.66
Pseudomonas
aeruginosa 0 (0.00) 4 (4.71) 0 (0.00) 0.57 1 (3.85) 0 (0.00) 3 (13.64) 0.02
Salmonella
enterica 0 (0.00) 3 (3.53) 0 (0.00) 0.65 1 (3.85) 2 (3.33) 0 (0.00) 0.67

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other areas (50.00%), and in the case of P. mirabilis, it was
23.08%, 15.00%, and 18.18%, respectively.
ELISA andmolecular assessment ofbacterial
pathogens
We assessed the specific antibodies in the plasma of rodents
by ELISA and no IgG antibodies were detected against Bru-
cella spp. C. abortus and C. burnetii (0%, N = 148, 95%CI:
0–0.024). The visceral samples were negative for C. burnetii,
Leptospira spp., Rickettsia spp., and Y. pestis (0%, N = 108,
95%CI: 0–0.03) by PCR. The fleas were also negative for C.
burnetii and Y. (0%, N = 18, 95%CI: 0–0.18). Furthermore,
six flea pools (31.58%, N = 19, 95%CI: 12.58–56.55) and
one mite pool (1/1) were positive for Rickettsia spp.
Antimicrobial resistance profile
AMR patterns were varied among the isolates. Out of
the 110 bacterial isolates, 31 isolates (28.18%, 95%CI:
20.02–37.56), which were E. coli only, did not show resist-
ance to any of the tested antimicrobials. Thirty-six isolates
(32.73%, 95%CI: 24.08–42.33) were resistant to 1–2 anti-
microbials, which includes E. coli (n = 14), P mirabilis
(n = 9), and K. pneumoniae (n = 6). The rest 43 (39.09%,
95%CI: 29.93–48.86) isolates, which were from 12 (n = 13,
92.31%, 95%CI: 63.97–99.8) bacterial species, were identi-
fied as MDR (Table4). The MDR bacteria were resistant
to 17 antimicrobials (85%, n = 20, 95%CI: 62.11–96.79),
whereas all bacterial isolates were sensitive to neomycin,
and pradofloxacin. Over 50% of the MDR isolates were
resistant to ampicillin, cefalotin, doxycycline, nitrofurantoin,
and tetracycline. The resistance pattern among the MDR
bacteria varied between three to nine antimicrobials. The
highest resistance were byP. stuarti (n = 1), E. coli (n = 3),
and P. merabilis (n = 1), which were resistant to 9 antimi-
crobials; followed by P. aeruginosa (n = 1), Salmonella
enterica (n = 2), resistant to 8 antimicrobials; and P. stuarti
(n = 1), resistant to 7 antimicrobials. Although the majority
of the MDR pathogens were isolated from agricultural facili-
ties (n = 28), there was no significant correlation (p = 0.14)
among MDR pathogens isolated from different facilities.
Similarly, the majority of the MDR isolates were from R.
norvegicus, and there was no significant difference (p = 0.92)
among MDR pathogens isolated from different rodent hosts.
Two (22.2%, 95%CI: 2.81–60.01) K. pneumoniae and seven
(11.86%, 95%CI: 4.91–22.93) E. coli were ESBL producers.
All ESBL producing bacteria were isolated from R. norvegi-
cus, although there was no significant correlation (p = 0.33)
between the ESBL producing pathogens and the location of
rodent trapping.
Discussion
The presence or absence of a disease, pathogen, or a vector
plays a major role in the success of any disease surveillance
program (Mohammed etal. 2015). Rodents are sources of
various pathogens in humans and animals (Han etal. 2015;
Meerburg etal. 2009). To the best of our knowledge, this is
the first study to identify and characterize bacterial species
from rodents in Qatar. We have reported 13 bacterial species,
the majority of which were isolated from rodents captured
in livestock farms. The livestock farms in Qatar are usually
managed with insufficient biosecurity measures. Different
domestic and exotic animals and birds are kept together in
the same enclosures, where the shepherds also live on the
farm premises. There are resting places (majlis) in the farms,
where the owners visit during their leisure time (Farag etal.
2018). A previous report from Qatar revealed that around
80% of livestock farms were infested with rodents (Nourel-
din and Farrag 2010). Infectious bacteria can infect humans
and other animals by direct or indirect exposure (Taylor etal.
2001). As such, keeping multi-species along with human
dwellers within the same enclosures can increase the risk
of cross-species transmission of infectious diseases (Rogdo
etal. 2012).
As the majority of the rodents were R. norvegicus and
were captured from the livestock farms, the relationship
with the isolated bacteria, AMR pattern, or ESBL produc-
tion with the rodent host or location of trapping may not
give an accurate picture of Qatar in our study. Among the
13 bacterial species, the prevalence of E. coli was high
(54.63%), which was substantially lower than that reported
in a previous study on livestock animals (88.7%) in Qatar
(Alhababi etal. 2020). In Saudi Arabia, the recovery rate of
E. coli from chicken was 31.1% (Altalhi etal. 2009). Rodent
fecal samples showed 75% and 4.8% positivity for E. coli
in Cyprus [46] and Singapore [47], respectively. E. coli is
a commensal bacterium in the animal intestine, and we did
not identify the pathogenic strains of E. coli in our study.
Methodological differences can also result in variations in
bacterial recovery rates (Ong etal. 2020). Therefore, E.coli
recovery in this study may be less important as pathogenic
strains of E. coli were not identified (Ramos etal. 2020).
Rodents are overlooked reservoirs of Brucella abortus,
Brucella melitensis, and C. burnetii, which has both human
and animal health importance (Abdel-Moein and Hamza
2018; Doosti and Moshkelani 2011; Psaroulaki etal. 2014;
Tiller etal. 2010). Rickettsia spp. are the causal agents of
spotted fever and typhus fever. Several vectors of Rickettsia
spp. have been reported in Qatar, such as Xenopsylla cheo-
pis, Ctenocephalides felis, and Ornithynyssus bacoti (Armed
Forces Pest Management Board 1999). Rodents and their
ectoparasites can act as reservoirs for Rickettsia spp. (Han

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Table 4 Multidrug resistant gram-negative bacteria isolated from rodent intestine and their resistant pattern
Bacterial Isolates Acinetobac-
ter bauman-
nii (n = 2)
Citrobac-
ter freundii
(n = 2)
Citrobac-
ter koseri
(n = 1)
Entero-
bacter
aerogenes
(n = 1)
Enterobac-
ter cloacae
(n = 1)
Escheri-
chia coli
(n = 14)
Hafnia
alvei (n = 1)
Klebsiella
pneumoniae
(n = 3)
Proteus
mirabilis
(n = 10)
Providencia
stuartii
(n = 2)
Pseu-
domonas
aeruginosa
(n = 3)
Salmonella
enterica
(n = 3)
Total MDR
species
(n = 43)
Antimicrobials
Amikacin 3 1
Amoxicillin/ Cla-
vulanic Acid
1 2 1 1 5 1 2 1 3 9
Ampicillin 1 11 1 3 1 2 3 2 8
Cefalotin 2 1 1 3 1 2 6
Cefovecin 1 1 2
Cefpodoxime 2 1 1 1 7 2 1 3 8
Ceftiofur 2 1 1 1 6 1 3 7
Chloramphenicol 1 1 1 1 2 1 1 7
Doxycycline 2 6 2 3
Enrofloxacin 5 1 1 4 1 2 1 7
Gentamicin 1 2 3 3
Imipenem 3 2 5 2 4
Nitrofurantoin 1 1 1 2 1 3 10 2 2 3 10
Piperacillin 3 3 2
Tetracycline 10 1 10 2 3 3 6
Tobramycin 2 1 2
Trimethoprim/
Sulfamethoxa-
zole
10 2 3 3
Total antimicrobials 7 4 4 5 3 14 6 7 12 7 9 10

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1 3
etal. 2015; Meerburg etal. 2009; Rabiee etal. 2018). In
the current study, we found Rickettsia spp. in rodent-borne
fleas and mites, which is reported for the first time among
humans and animals in Qatar. Although there is no previous
report of rickettsial disease in humans or animals in Qatar,
the country is at risk of this pathogen when considering the
close interaction between humans and animals. Leptospiro-
sis is also a rodent-borne disease, which is commonly seen
in flood-prone areas and among those people who are in
constant contact with animals (Naing etal. 2019). In Qatar,
the majority of residents and animal shepherds are from the
Indian subcontinent (Priya D’Souza Communations 2019;
Social & Economic Survey Research Institute 2021), where
leptospirosis is commonly seen (Victoriano etal. 2009).
Hence, we tested for the presence of this disease in the
Qatari rodents. Plague is a reemerging disease in the WHO
Eastern Mediterranean region (Mostafavi etal. 2021). There
were three outbreaks of bubonic plague in this region; two
in Lebanon and one in Afghanistan in the last two decades.
Rodents and rat flea (Xenopsylla astia) act as reservoir of
Y. pestis (Dennis 1999; Mahmoudi etal. 2020). Our study
revealed that Brucella spp., C. abortus, C. burnetii, Lepto-
spira spp. and Y. pestis were not present in our sample of
rodents in Qatar.
The bacterial pathogens that we identified are primarily
found in soil and water, and sometimes as normal flora of
the animal intestine (Brown etal. 2012). They have oppor-
tunistic pathogenic dynamics in humans and animals (Brown
etal. 2012; Done and Radostits 2007), causing infections
associated with community-based and healthcare settings,
especially in pediatric, elderly, and immunocompromised
patients, resulting in gastroenteritis, urinary tract infection
(UTI), pneumonia, and sepsis (Choi etal. 2015; Gillespie
1994; Levinson 2018; Tomas 2012; Wie 2015). Some of
these pathogens have been identified in patients of differ-
ent hospital settings in Qatar. E. coliand Salmonella spp.
are common causes of human gastroenteritis in Qatar (Ghu-
naim etal. 2015; Humphrey etal. 2016; Mohammed etal.
2015). Acinetobacter baumannii was isolated from hospital-
ized adult patients and caused pneumonia (Al Samawi etal.
2016). C. fruendii, Enterobacter aerogenes, Enterobacter
cloacae, E.coli, and K. pneumoniae were detected in the
intensive care unit patients. Pediatric patients with UTI were
positive for Citrobacter koseri and E. cloacae. Similarly, P.
aeruginosa was isolated from hospitalized patients in Qatar
(Sid Ahmed etal. 2020). Moreover, Escherichia, Klebsiella,
Pseudomonas, and Salmonella cause enteritis, pneumonia,
mastitis, and septicemia in livestock animals (Done and
Radostits 2007). Acinetobacter, Aeromonas, and Proteus
are also pathogenic to animals (Askari etal. 2019; Schuk-
ken etal. 2012). It is possible to transmit these pathogens
from animals to humans through tainted animal products for
human consumption (Guerra etal. 2014).
AMR occurs when a pathogen changes over time and
does not respond to antimicrobials. It makes an infection
difficult to treat, thereby increasing the risk of spread-
ing disease, severe illness, and death. AMR organisms
are found in nature, which usually occur through genetic
changes and spread at the human-animal-environment
interface (Khan etal. 2020). The major drivers of AMR
are the misuse and overuse of antimicrobials; inadequate
access to clean water; lack of proper sanitation and hygiene
for humans and animals; poor infection and disease pre-
vention and control (IP&C) in healthcare and farm set-
tings; poor access to medical services; lack of awareness,
knowledge, and related legislation (Hassan etal. 2021;
Kalam etal. 2021; World Health Organization 2015). This
study examined the antimicrobial resistance to 20 antimi-
crobials agents to reveal the drug resistance patterns of
gram-negative gut bacteria in commensal rodents of Qatar.
Many microbes in the environment can have natural resist-
ance to some of these antibiotics (Nair etal. 2011). Of the
isolated bacteria in this study, six were from the ESCAPE
group. ESCAPE, stands for Enterococcus faecium, Staphy-
lococcus aureus, Clostridium difficile, A. baumannii, P.
aeruginosa, and E refers to Enterobacteriaceae including
E. coli, K. pneumoniae, Proteus spp., and Enterobacter
spp., are generally MDR pathogens (Akova 2016). Our
study found that several K. pneumoniae and E. coli were
ESBL producers, which affirming a previous finding that
mentioned that CTX-M-1 gene in E. coli and K. pneu-
moniae is responsible for ESBL production in Qatar (Sid
Ahmed etal. 2016). ESBL can make a pathogen resist-
ant to cephalosporins, carbapenems, and aminoglycosides
(Ghafourian etal. 2015; Paterson and Bonomo 2005; Sawa
etal. 2020). In this study, the majority of MDR E. coli
strains were resistant to ampicillin, tetracycline, and tri-
methoprim/sulfamethoxazole. More than 50% of E. coli
from chickens in Saudi Arabia showed resistant to ampi-
cillin, chloramphenicol, gentamycin, tetracycline, and tri-
methoprim/Sulfamethoxazole (Altalhi etal. 2009). Over
50% resistance to ampicillin, cefalotin, and tetracyclin
was reported for E. coli isolated from chicken in Qatar
(Johar etal. 2021). Over 50% of P. mirabilis in this study
were resistant to doxycycline and tetracycline, which is
in accordance with the statement by Stock (Stock 2003),
who indicated that P. mirabilis can be naturally resistant to
these antimicrobials. However, Stock showed that P. mira-
bilis could be naturally sensitive to nitrofurantoin, whereas
in our study, there was major resistance (89%) against this
antimicrobial. Due to the lack of guidelines and ambigu-
ous regulations regarding antibiotic use among animals in
veterinary practice, there are chances of increased anti-
microbial resistance among animals (Gillings 2013). As
most livestock farms keep mixed species animals with
poor biosecurity management, there is a chance to cross

Veterinary Research Communications
1 3
the species barrier by MDR pathogens between rodents
and other animals, including humans.
Our study suggests that rodents can serve as a source of
zoonotic bacteria at the human-animal-environmental inter-
face. Raising caution within the community and implement-
ing appropriate preventive measures can help to alleviate
the burden of vector-borne diseases (Desoky 2018; Núñez
etal. 2014). These measures can include maintaining proper
hygiene, enhancing biosecurity and farm management in the
animal and agricultural farmsteads, and appropriate IP&C in
hospital settings. The limitations of the current study were
that we did not determine the pathogenic potential of the
isolates and concentrated only on gram-negative bacteria;
therefore, the gram-positive enteric bacteria, such as Fuso-
bacterium or Bacteroides, were not analyzed. Additionally,
we only used aerobic culture methods, which is why we did
not detect any anaerobic bacteria, such as Clostridium spp.
Conclusions
This study constitutes the first report of rodent-borne bac-
terial investigation in commensal rodents in Qatar. These
isolates include A. baumannii, A. salmonicida, Citrobacter
freundii, C. koseri, E. aerogenes, E. cloacae, Hafnia alvei,
K. pneumoniae, P. stuartii, P. mirabilis, and P. aeruginosa,
which were first time reported in rodents. Our study shows
that rodents are potential sources of zoonotic and opportun-
istic bacterial pathogens at the human-animal-environmental
interface in Qatar. The risk increases if MDR pathogens
cross the species barriers and infect humans and other ani-
mals. Particularly in the latter case, animal and agricultural
farms can serve as sources of such pathogens. Therefore,
farm biosecurity measures must be implemented in animal
and agricultural settings to avoid such pathogenic transmis-
sion. We recommend conducting further studies for molecu-
lar characterization of these pathogens.
Acknowledgments The authors acknowledge the Department of Ani-
mal Resources, Qatar, for providing laboratory facilities to conduct
the study. The authors are thankful for the support of Mr. Sowaid Ali
Almalki, Dr. Randa Abdeen, Mr. Gulam Dastagir Syed, and Mr. Newaj
Abdul Majeed in this research work. Thanks to Ms. Lynne M. Fraser
of Qatar National Library for her support in the English editing of this
manuscript.
Data availability All data are available with the first author.
Author contributions Conceptualization, MMI, EF, and ZM-K; meth-
odology, MMI, KAE, MSK, MA, MKS, AMA-M; formal analysis,
MMI and MMH;writing—original draft preparation, MMI, MMH,
DB, and ZM-K; writing—review and editing, MMI, MMH, EF, DB,
KAE, HMY,and ZM-K; visualization, AAS, EF, and ZM-K; supervi-
sion, EF and ZM-K; project administration, HA-R, AMA-M, AAA-Z,
andEF; funding acquisition, EF AAS, and HA-R. All authors have read
and agreed to the published version of the manuscript.
Funding The research was funded by the Ministry of Public Health,
Qatar.
Declarations
Ethical permission The current study is a part of the “Risk assessment
of rodent-borne zoonotic diseases in Qatar” project. Ethical approval
was obtained from the Institutional Animal Care and Use Committee
of the Ministry of Municipality and Environment, the State of Qatar
(IACUC-A-MME-4) to conduct the study.
Conflict of interest The authors declare no conflict of interest.
Consent to participate and consent for publication All authors attended
in the work and accepted the manuscript to publish.
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Authors and Aliations
MdMazharulIslam1,2 · ElmoubasharFarag3· MohammadMahmudulHassan4 · KhalidA.Enan1,5·
K.V.MohammadSabeel1· MaryamMohammedAlhaddad1· MariaK.Smatti6· AbdullaMohammadAl‑Marri1·
AbdulAziaAl‑Zeyara1· HamadAl‑Romaihi3· HadiM.Yassine6· AliA.Sultan7· DevendraBansal3·
ZilungileMkhize‑Kwitshana2,8
Elmoubashar Farag
eabdfarag@moph.gov.qa
Mohammad Mahmudul Hassan
miladhasan@yahoo.com
Khalid A. Enan
khalid.enan@gmail.com
K. V. Mohammad Sabeel
sabeel84@gmail.com
Maryam Mohammed Alhaddad
maryamalhaddad12@gmail.com
Maria K. Smatti
msmatti@qu.edu.qa
Abdulla Mohammad Al-Marri
abmmarri@mme.gov.qa
Abdul Azia Al-Zeyara
amzeyara@mme.gov.qa
Hamad Al-Romaihi
halromaihi@moph.gov.qa
Hadi M. Yassine
hyassine@qu.edu.qa
Ali A. Sultan
als2026@qatar-med.cornell.edu
Devendra Bansal
dbansal@moph.gov.qa
Zilungile Mkhize-Kwitshana
mkhizekwitshanaz@ukzn.ac.za
1 Department ofAnimal Resources, Ministry ofMunicipality
andEnvironment, Doha, Qatar
2 School ofLaboratory Medicine andMedical Sciences,
College ofHealth Sciences, University ofKwaZulu Natal,
Durban4000, SouthAfrica
3 Ministry ofPublic Health, Doha, Qatar
4 Faculty ofVeterinary Medicine, Chottogram Veterinary
andAnimal Sciences University, Khulshi, Chattogram4225,
Bangladesh
5 Department ofVirology, Central Laboratory, The Ministry
ofHigher Education andScientific Research, 7099Khartum,
Sudan
6 Biomedical Research Center, Qatar University, Doha, Qatar
7 Department ofMicrobiology andImmunology, Weill Cornell
Medicine, Cornell University, Doha, Qatar
8 Division ofResearch Capacity Development, South African
Medical Research Council, Tygerberg, CapeTown7505,
SouthAfrica