Journal of Advances in Microbiology

6(4): 1-7, 2017; Article no.JAMB.36715

ISSN: 2456-7116

Bacterial Resistance to Antibiotics: Current

Situation in Sudan
Abeer M. Abass1, Muna E. Ahmed1*, Ishraga G. Ibrahim2 and S. A. Yahia1
1
Department of Bacteriology, Central Veterinary Research Laboratory, Alamarat, Animal Resources
Research Corporation, Khartoum, Sudan.
2
Department of Chemistry, Central Veterinary Research Laboratory, Alamarat, Animal Resources
Research Corporation, Khartoum, Sudan.

Authors’ contributions

This work was carried out in collaboration between all authors. Author AMA designed the study and
managed the literature searches. Authors MEA and IGI managed the literature, wrote the protocol,
and wrote the first draft of the manuscript. Author SAY analyzed the results and revised the
manuscript. All authors read and approved the final manuscript.

Article Information

DOI: 10.9734/JAMB/2017/36715
Editor(s):
(1) Ana Claudia Correia Coelho, Department of Veterinary Sciences, University of Trás-os-Montes and Alto Douro, Portugal.
Reviewers:
(1) Abimbola Olumide Adekanmbi, University of Ibadan, Nigeria.
(2) Yasmine Samy Moustafa Mohammed Ali, Egypt.
(3) Mohamed Mohamed Adel El Sokkary, Mansoura University, Egypt.
(4) Falodun Olutayo Israel, University of Ibadan, Nigeria.
Complete Peer review History: http://www.sciencedomain.org/review-history/21861

Received 11th September 2017

th
Review Article Accepted 6 November 2017
Published 11th November 2017

ABSTRACT

Aims: This work was conducted to evaluate the antimicrobial resistance of Gram positive and Gram
negative bacteria of human and animal origin to commonly used antibiotics in Sudan according to
the previous studies on antimicrobial resistant.
Study Design: Data were collected from relevant studies for both human and animal sectors
published during 2001 to 2017 and met the inclusion criteria. Examined samples includes: serum,
urine, milk, stool, abscesses and tissue sample.
Place and Duration of Study: This study was carried out in Khartoum State Sudan during 2016-
2017.
Methodology: The data collected in this study were obtained from different educational institution
and research centers located in Khartoum State and previous reports related to antimicrobial
resistant.

_____________________________________________________________________________________________________

*Corresponding author: E-mail: mna2tt@gmail.com;

 Abeer et al.; JAMB, 6(4): 1-7, 2017; Article no.JAMB.36715

Results: Escherichia coli (E. coli) Klebsiella spp. Proteus spp. Klebsiella pneumoniae,
Pseudomonas aeruginosa, Staphylococcus aureus, Mycobacterium tuberculosis (M. tuberculosis)
and Salmonella enteritidis (Sal. enteritidis) were the most commonly encountered organism. Most of
the studied organisms were highly resistance to: chloramphenicol, penicillin, amoxicillin,
erythromycin, tetracycline, ampicillin (10%), sulbactam, cefotaxime (30%), nitrofurantoin, nalidixic
acid, colistin sulphate and streptomycin, vancomycin, imipenem, amikacin (30%), and tobramycin.
While Ciprofloxacin, norfloxacin, gentamicin (30%), and Linezolid were the antibiotics with the
highest activity against isolated organism.
Conclusion: The currently data, suggested that the antimicrobial susceptibility and resistance of
most common Gram positive and Gram negative organisms causing diseases are similar to other
countries. Clinicians should be aware of the existing data and treat patients according to the
susceptibility patterns. Further studies are wanted from all over the country because there is limited
published data.

Keywords: Antibiotics; resistant; bacteria; gram positive; gram negative; Sudan; current.

1. INTRODUCTION Bacteria can have intrinsic (natural) to resistant

Antimicrobial resistance has been detected in all
parts of the world; it is one of the greatest
challenges to global public health today, and the
problem is increasing. It is now accepted that
increased antimicrobial resistance (AMR) in
bacteria affecting humans and animals in recent
decades is primarily influenced by misuse and
over use of antimicrobials for a variety of
purposes (O’Neill, 2015). While AMR can occur
naturally through adaption of microorganisms to
their surrounding environment, it is exacerbated
by inappropriate and excessive use of
antimicrobials. There are a range of factors
which have contributed to this such as lack of
regulation, poor therapy adherence, non-
therapeutic use and over-the-counter sales and
poor husbandry, hygiene and agricultural waste
management. The containment of AMR requires
a global approach combined with concerted
actions at the national level. For tackling AMR a
global action plan was developed by WHO in
collaboration with OIE (animal health) and FAO
(agriculture) (Tripartite partnership) toward “One
Health Approach”.
Antibiotic resistance is defined as the ability of a
micro-organism to grow or survive in the
presence of an antibiotic that is usually sufficient
to inhibit or kill microganisms of the same
species [1]. Antimicrobial resistance patterns are
continually evolving and Multidrug resistance
(MDR) organisms undergo progressive
antimicrobial resistance, therefore, continuously
updated data on antimicrobial susceptibility
profiles is essential to ensure the provision of
safe and effective empiric therapies.
antibiotics or they can develop acquired
resistance to antibiotics [2]. Intrinsic resistance is
the natural ability of bacteria to be resistant due
to inherent structural or biochemical features of
the bacteria. Knowing which bacteria were
naturally resistant to particular antibiotics helps
veterinarians and clinicians to prescribe
appropriate and effective treatments. Bacteria
can become resistant through the acquisition of
foreign DNA originally from other bacteria, e.g.
via plasmids (small circular DNA strands), in a
process called Horizontal Gene Transfer (HGT).
Sometimes these genetic mutations or the
acquisition of foreign resistance genes can lead
to the emergence of bacteria with an improved
ability to survive treatment with particular
antibiotics [2].
In Sudan most of the studies in the area of
antibiotic use and antimicrobial resistance are
carried out by individual researcher because
of personal interest and /or for academic
awards rather than being guided by national
research priorities and needs. These studies in
human and agriculture sectors are scarce,
fragmentary, and riddled with gaps and no AMR
surveillance on country wise was conducted
[3,4].
2. CURRENT SITUATION OF AMR IN
SUDAN
Sudan total population was approaching forty
million and livestock hold was estimated to be
107 million head of a diverse species including
cattle, sheep, goats and camels (FMOH, 2014;
MOAR, 2016).

2

The antimicrobial use (AMU) is not regulated and
Antimicrobials can be easily obtained over the
counter from pharmacies, general stores and
market stalls. No maps of antimicrobials sales
and distribution pathways are available now,
Furthermore, no specific guidelines on AMU.
The data discussed in this Manuscript were
collected from different studies carried out using
different methodologies.
The antibiotic sensitivity test was conducted on
some Escherichia spp., isolated from intestinal
samples from healthy camels, sheep, goats and
poultry against eight antimicrobial agent, namely
co-trimexazole, nalidixic acid, nitrofurantoin,
ampicillin, tetracycline, gentamicin, colistin
sulphate and streptomycin. All the isolates were
sensitive for co-trimexazole, nalidixic acid,
nitrofurantoin, gentamycin, streptomycin,
tetracycline and colistin sulphate except in sheep
(they were resistant to ampicillin). In camels (E.
coli, E. hermannii, and E. adecarboxylate) were
highly susceptible to nitrofurantoin, nalidixic acid,
co-trimexazole, ampicillin and gentamycin, and
showed intermediate susceptibility to colistin
sulphate, but were resistant to tetracycline and
streptomycin [5].
A study by Saeed [6] investigated resistances
of five strains of Klebsiella pneumoniae
(K. pneumoniae), Eschericia coli (E. coli),
Pseudomonas. Aeruginosa (Ps. Aeruginosa),
Staphylococcus aureus (S. aureus) and six
strains of Salmonella spp. to the six antibiotics,
they were; ciprofloxacin, erythromycin,
amoxicillin, cephalexin and cephradine. It was
found that ciprofloxacin was the most effective
drug against all the organisms tested even at a
very low concentration (0.781 µg/mL), but all the
Gram-negative bacteria were found to be
resistant to erythromycin. Ps. aeruginosa was
found to be resistant to chloramphenicol.
Fagir [7] studied the prevalence of vancomycin
resistant Enterococcus spp. in clinical samples
(urine, wound swab specimens and stool) of
carriers of both hospitalized and non-hospitalized
patients in Khartoum state. The result showed
that Enterococcus spp. isolates were resistant
to several antibiotics used in this study, but
were susceptible to imipenem and
chloramphenicol.
Also in a study in Khartoum State, one hundred
and fifteen samples and swabs were collected
from infected human, wound, abscesses,
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Abeer et al.; JAMB, 6(4): 1-7, 2017; Article no.JAMB.36715
infected ear, infected equine uterus, milk from
mastitis cows and goat's and infected poultry
tissues. The sensitivity of 98 isolates to twenty
one antimicrobial drugs was examined. (92.9%)
Staphylococcus spp and (88.9%) of
Enterobacteriacea were highly resistant to
ampicillin. The Streptococcus spp. and
Corynebaterium spp. were completely resistant
to nalidixic acid and methicillin.
Enterobacteriacea spp. and Pseudomonas spp.
were completely resistant to penicillin and
vancomycin .While (87.7%) of Staphylococcus
spp were resistant to penicillin. (85.7%) of
Streptococcus spp were resistant to pencillin.
Also, Streptococcus spp were completely
resistant to colistin sulphate, co-trimoxazole,
methicillin and clindamycin. Multi drug resistance
was shown by most of bacteria strains isolated.
The multiple drug resistance observed varied
from two-drug- multiple resistances (ampicillin,
penicillin) to eleven multiple drugs resistances
(ampicillin, streptomycin, cloxacillin, penicillin,
vancomycin, rifampicin, erythromycin, methicillin,
tetracycline, cephalothin and clindamycin [8].
Also Elabbas [9] screened the antibiotics
sensitivity test of 15 (Sal. enteritidis) isolated
from fecal samples of chickens suffering from
diarrhea in Khartoum State, Each isolate was
tested against ten antimicrobial agents amikacin,
ceftizoxime, ciprofloxacin, gentamicin, ampicillin,
sulbactam, piperacillin, tazobactam, cefotaxime,
chloramphenicol, tetracycline and co-
trimexazole. All of the isolates were sensitive to
the tested drugs, except tetracycline and co-
trimexazole.
Mohammed Noor [10] tested antimicrobial
sensitivity of (200) isolates of M. tuberculosis
complex against 4 drugs; Isoniazid. rifampicin,
streptomycin and Ethambutol. Only 67(33.5%)
isolates were sensitive to the four drugs, Mono-
drug resistance was as follows; 35(17.5%)
isolates were resistant to Isoniazid, 31(15.5%)
were resistant to rifampicin, 43(21.5%) were
resistant to streptomycin and 24(12%) were
resistant to Ethambutol, While the multi-drug
resistance was as follows: 12(6%) isolates were
resistant to Isoniazid and rifampicin, 5(2.5%)
were resistant to three drugs and 9(4.5%) were
resistant to the four drugs.
Also antimicrobial sensitivity test was carried out
for all E. coli isolates in diarrheic chickens
against ten commonly used antibacterial agents.
All isolates were sensitive to amikacin (30 mcg)
and ceftizoxime (30%) and resistant to

tetracycline, ampicillin (10 mcg), sulbactam, co-
trimoxazole (25%), piperacillin, tazobactam and
cefotaxime (30%). The isolates showed different
pattern of antibiotic susceptibility to other
antimicrobial agent; 88% of the isolates were
sensitive to ciprofloxacin, 68% were sensitive to
gentamycin (30%) and 27% were sensitive to
chloramphenicol [11].
Another studies, also looking at susceptibility of
S. aureus isolated from wounds, skin, blood and
urine samples to ciprofloxacin, norfloxacin [12].
Erythromycin and azithromycin [13,14] it was
found that the organism showed 80%, 86%,
96.7%, 96.7% and 76.7% respectively while 70%
of tested strains showed a high resistant to
amoxicillin [14].
Ibrahim and colleagues [15], determined the
prevalence and susceptibility of MDR E. coli
isolated from clinical patients in hospitals at
Khartoum State. E. coli (n = 232) isolated from
specimens, identified and tested their
antimicrobials susceptibility, the results showed
that, of the 232 E. coli isolates, the majority were
from urine (65.1%). MDR E. coli were present in
214 (92.2%). Of these, the resistance rates were
recorded to amoxicillin 97.7%, cefuroxime
92.5%, trimethoprim-sulfamethoxazole 88.3%,
tetracycline 77.1%, nalidixic acid 72%,
ceftriaxone 64%, ciprofloxacin 58.4%, ofloxacin
55.1%, amoxicillin-clavulanate 50.4%,
ceftazidime, gentamicin 35% each, nitrofurantoin
22.4%, chloramphenicol, tobramycin 18.2% each
and amikacin 1.9%. Overall MDR E. coli, 53.3%
were resistant to > 7 antimicrobial agents
Isolates from males were more resistant than
those from females (p < 0.05).
A total of 64 Salmonella spp. isolates belonging
to 28 different serovars were tested for their
susceptibility to 13 antimicrobial agents. The
Isolates were frequently resistant to ampicillin
(90.6%), cephalexin (50.0%), nalidixic acid
(25.0%), streptomycin (21.9%), kanamycin
(18.8%), gentamicin (17.2%), and co-trimoxazole
and trimethoprim (12.5%). The most common
pattern of multiple drug resistance included
resistant to ampicillin and cephalexin. Most
isolates were sensitive to chloramphenicol
(98.4%), ciprofloxacin (93.8%), and norfloxacin
(90.6%). Two chicken- and the two human-
origin S. Kentucky isolates were resistant to
both ciprofloxacin and norfloxacin. All S.
Kentucky isolates and the one S. Rissen
isolates demonstrated multi-drug resistance
[16].
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Abeer et al.; JAMB, 6(4): 1-7, 2017; Article no.JAMB.36715
Alsmmani `and colleagues [17] identified
bacterial uropathogens that responsible for
urinary tract infection (UTIs) in children less than
5 years age, and determined the antibiotic
resistance of the isolates to commonly used
antibiotics. The result showed that E. coli was the
most common uropathogen, of which 23(42.6%)
were sensitive to ciprofloxacin (91.3%) and
resistant to augmentin (91.3%) and
cotrimoxazole (100%), followed by 16(29.6%) Ps.
aeruginosa which were sensitive to ciprofloxacin
(75%) and norfloxacin (68.8%), and resistant to
cephalexin (81.2%), 10(18.5%) K. pneumoniae
were sensitive to Ciprofloxacin and norfloxacin
and nalidixic acid (90%) and resistant to
nitrofurantoin (100%) and 5(9.3) Proteus mirabilis
were sensitive to ciprofloxacin and norfloxacin
(90%), amoxicillin / clavulanic acid and
augmentin (80%).
In another study, susceptibility of sixty E. coli
isolates were determined to: two beta lactams;
amoxicillin, cephalexin and two fluoroquinolones;
(norfloxacin and ciprofloxacin) to each agent
individually and then to a combination of
amoxicillin with norfloxacin and cephalexin with
ciprofloxacin. The isolates were resistant to
amoxicillin and after the combination with
norfloxacin the resistance was 20%; the
norfloxacin showed 35% and 29% before and
after respectively. In case of ciprofloxacin after
combination with cephalexin the resistance
dropped from 40% to 18.3%. These findings
serve to consider the effect of combinations of
antibiotics in strengthening their effects;
increasing the susceptibility and decreasing the
resistance [18].
Antibiotic sensitivity test was performed by Muna
et al. [19] using Vitek 2 Compact in which a
total of 800 affected lung samples from 400
camels (Camelus dromedarius) were collected of
which, 713 bacterial isolates were collected from
the specimens, 489 (68.6%) were Gram positive
and 224 (31.4%) were Gram negative. In
addition, antimicrobial resistance were
determined and the result revealed that, Gram
positive bacteria: S. aureus, S. epidermidis, S.
simulans, S. chromogens and Enterococcus
faecalis (En. faecalis) were resistant to
benzylpencillin, S. haemolyticus, Enterococcus
faecalis (En. faecalis) were resistant to ampicillin.
S. aureus, S. chromogens were resistant to
oxacillin, S. aureus, S. epidermidis, S. simulans
and En. faecalis were resistant to erythromycin
and clindamycin, S. simulans was resistant to
vancomycin, S. haemolyticus, S. aureus, S.

epidermidis and S. intermedius were resistant to
tetracycline, S. haemolyticus and En. faecalis
were resistant to sulphamethazole and
trimethoprim. Gram negative organism
Burkholderia cepacia (B. cepacia), E. coli and
Ps. aeruginosa were resistant to ampicillin and
nitrofurantoin, B. cepacia, E. coli and Ps.
aeruginosa were resistant to cefoxitin. B. cepacia
and E. coli were resistant to imipenem, amikacin,
and tobramycin.
Recent Hussein [20] reported the genome
sequence of a multidrug-resistant Ps. aeruginosa
strain isolated from a patient with a urinary tract
infection in 2015.
Another study carried out by Solima [21] to
detect the prevalence of first-line tuberculosis
(TB) drug resistance among a group of
previously treated and newly detected TB
patients, to determine the association between
prevalence of multidrug resistance (MDR) and
demographic information (age and sex), to
explain genes correlated with MDR M.
tuberculosis, and to characterize multidrug
resistant tuberculosis (MTB) via 16S ribosomal
RNA (16S rRNA) analysis. Samples were
collected from a hundred MTB isolates from
Sudanese pulmonary TB patients. The
proportional method of drug susceptibility test
was carried out on Lowenstein-jensen media.
Multiplex PCR of rpoB and KatG genes and inhA
promoter was conducted; then rrs genes were
amplified by conventional PCR and were
sequenced. The sequences of the PCR product
were compared with known rrs gene sequences
in the Gene Bank database by multiple sequence
alignment tools. The result revealed that, the
prevalence of MDR was 14.7% among old cases
and 5.3% among newly diagnosed cases.
MDR organisms were analyzed for carriage of
common resistance genes (TEM, SHV, CTXM,
VIM, NDM1, qnr etc.) A study done by Malik [22]
on characterization of extended-spectrum ß-
lactamases (ESBLs) in cefotaxime and/or
ceftazidime multidrug resistant enterobacterial
pathogens as well as commensal isolates
collected in Sudan during the period 2002-2003
were tested for ESBL production which was
determined phenotypically by the combined disc
method, and was characterized genotypically by
the detection of bla genes by PCR and
nucleotide sequencing. Transferability was
examined by conjugation with nalidixic-acid
resistant E.coli K12. In another study, on the
prevalence and characterization of antibiotic
5
Abeer et al.; JAMB, 6(4): 1-7, 2017; Article no.JAMB.36715
resistance genes among Gram negative bacteria
by Musa [23]. He tested ESBL producing
Enterobacteriaceae, 181 strains of E. coli and
Klebsiella spp. from Soba University Hospital
(SUH) and 206 similar strains from Khartoum
Teaching Hospital (KTH) for the presence of
resistance genes. The study revealed that 61.9%
of E. coli and 83% of Klebsiella spp. were ESBL
producers and 11% of the strains were inducible
AmpC producers.
Alsadig et al. [24] confirms that the multi drugs
organisms’ infection was common in hospitalized
patients with diabetic foot ulcers in Libya. The
prevalence of MRSA isolates was higher in
liybian population as compared with previous
studies.
Recently Amir et al. in [25] state that several
studies in different countries show geographic
variations in etiologic agents of urinary tract
infections and their resistance patterns to
antibiotics however, in Sudan he found that
the most common urinary isolates were
highly resistant when they were tested
against ampicillin, amoxicillin, co-trimoxazole,
tetracycline, sulfonamide, trimethoprim,
streptomycin, and carbenicillin.
Also Ayman et al. in [26] reported the acceptable
current sensitivity patterns of Salmonella typhi
(S. typhi) isolates against ciprofloxacin, but the
probability of emerging multidrug resistance to
ciprofloxacin was observed in sensitivity which
had begun to decline according to frequent
consuming, drug policy and bacterial genetic
mutations.
To minimize conditions which may favour the
development of antibiotic resistance and to
reduce the chances of treatment failure, it is
important that antibiotics are taken correctly,
following the instructions for dosage and duration
of treatment. Some antibiotics need to reach a
particular concentration in the body
(concentration-dependent) or are provided for a
certain length of time (time-dependent) in order
to be fully effective. Importantly, sub-optimal
dosage or duration of antibiotic treatment is
important contributors to the development of
resistance. This is why it is essential that
treatment doses are calculated correctly and that
the treatment duration instructions are followed
exactly as directed by the vet who prescribed the
antibiotic. Drug-resistance surveillance and
epidemiological analysis of patient data is
needed periodically and can be informative for

appropriate management of antimicrobial
resistance.
Advances in genetics, genomics and computer
science will likely change the way that infections
and new types of resistance are diagnosed,
detected and reported worldwide so that we can
fight back faster when bacteria evolve to resist
drugs. These same technological advances will
deliver rapid diagnostic tools in the future to
improve the way we use the antibiotics [27].
The frequency of the organisms compare to the
tested samples could be hardly calculated
because many researchers work on clinical
samples that were found ready identified in the
isolate banks. In addition, some investigators did
not recorded the number of the samples tested
and also a lot of works had been done but not
published.
3. CONCLUSIONS
The containment of AMR requires a global
approach combined with concerted actions at the
national level. Further studies from other parts of
the country were needed since there is no or
limited published data available.
To control the antimicrobial resistance in Sudan,
Many factors contribute to the high prevalence of
antimicrobial resistance in Sudan, the most
significant of which is the antibiotic formulary.
Measures to control resistance, therefore, start
with correcting the formulary. Other measures
include education of healthcare workers,
implementation of infection control policies and
procedures.
COMPETING INTERESTS
Authors have declared that no competing
interests exist.
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