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J Islamabad Med Dental Coll 2019
8
Open Access
Commonly Occurring Bacteria in Diabetic Foot Infections and their
Sensitivity to various Antibiotics
Muneeb-ullah 1, Awais Saeed Abbasi 2, Seemab Niaz 3, Wajiha Mahjbeen 4
1, 2 Registrar, Accident and Emergency Department, Dr. Akbar Niazi Teaching Hospital (DANTH), Islamabad.
3Post Graduate Trainee, PIMS Hospital, Islamabad.
4Associate Professor, Chemical Pathology, DANTH, Islamabad
A B S T R A C T
Background: Diabetic foot infections are a common cause of morbidity in type 1 & 2 Diabetes mellitus. The selection of
appropriate empirical treatment is thus essential while treating such patients. The main objective of this study was to find out most
prevalent bacteria and their sensitivity to various antibiotics in patients with diabetic foot infections.
Material and Methods: This cross-sectional study was conducted in the Department of Surgery, Pakistan Institute of Medical
Sciences (PIMS), Islamabad from January 2017 to December 2017. A total 118 patients were included through consecutive
sampling technique. Samples were collected in the form of swab, pus or tissue material and were cultured on blood agar and
microorganisms were identified using standard microbiological methods. Antimicrobial sensitivity was also checked. Statistical
Package for Social Sciences (SPSS) version 22 was used to analyze data.
Results: Out of 118 patients, 72% (n=85) were males while 28% (n=33) were females. Cultures of 105 patients were positive and
most common organisms isolated were S. aureus (32.4%; n=34), E. coli (17.1%; n=18), P. aeruginosa (14.3%; n=15), Polymicrobials
(14.3%; n=15) and K. pneumoniae (7.6%; n=8). Antibiotics to which organisms were most sensitive included Piperacillin/Tazobactam
(69.5%; n=73), Imipenem (55.2%; n=58), Amikacin (43.8%; n=46), Vancomycin (40%; n=42) and Levofloxacin (38.1%; n=40).
Conclusion: Most common organisms causing diabetic foot infections in our study were S. aureus, E. coli, P. aeruginosa,
Polymicrobial and Klebsiella. Overall most sensitive antibiotics to these organisms included Piperacillin/Tazobactam, Imipenem,
Amikacin, Vancomycin and Levofloxacin.
Key words: Antibiotics, Diabetic foot infections, Escherichia coli, Pseudomonas aeruginosa, Piperacillin/Tazobactam,
Staphylococcus aureus
Authors’ Contribution:
1,2 Conception, synthesis, planning of
research and manuscript writing 3
Interpretation, discussion, Active
participation in data collection
4 Data analysis.
Correspondence:
Muneebullah
Email: muneebullah@gmail.com
Article info:
Received: March 24, 2018
Accepted: January 10, 2019
Cite this article. Muneeb-ullah, Abbasi AS, Niaz S, Mahjbeen W. Commonly occurring
bacteria in diabetic foot infections and their sensitivity to various antibiotics. J Islamabad
Med Dental Coll.2019; 8(1):8-12
Funding Source: Nil
Conflict of Interest: Nil
I n t r o du ction
The average worldwide prevalence of type 2 Diabetes
Mellitus in adults is 6.4 %. It ranges from 3.8 to 10.2%
among different regions of Pakistan. Rates of
undiagnosed diabetes may be as high as 50% in some
areas.1 Incidence of Type 1 Diabetes Mellitus also vary
worldwide with highest reported incidence in Finland and
Sardinia (37- 65 per 100,000) and lowest in China and
Venezuela (0.1-1.9 per 100,000).2,3 Foot related problems
are an important cause of morbidity in patients with
diabetes mellitus. Lifetime risk of foot ulcers for diabetic
patients (type 1 or 2) may be as high as 25%.4
Neuropathy, peripheral vascular disease (PVD) and poor
glycemic control are among the important risk factors
responsible for development of diabetic foot infection.5
ORIGI NA L A RT IC LE
J Islamabad Med Dental Coll 2019
9
Sensory neuropathy causes diminished perception of pain
and temperature that leads to poor recognition of injury to
the feet. Autonomic neuropathy causes reduced sweat
secretion resulting in dry, cracked skin that facilitates the
entry of microorganisms. Motor neuropathy leads to foot
deformities leading to pressure induced soft tissue
damage. Most of the diabetic foot infections are
polymicrobial and are variable depending on the extent of
involvement.5
Host defense and neutrophil functions are impaired by
hyperglycemia. Trauma in patients with one or more of
these risk factors precipitate development of wounds that
are slow to heal and predispose to secondary infection.
Three key steps involved in evaluation of a patient with
diabetic foot infection are: 1) identification of risk factors,
2) determination of extent and severity of infection and 3)
assessment of microbial etiology.5 For preventive and
monitoring strategies, certain risk categorization systems
can be used. One such system is developed by
International Working Group on the Diabetic Foot that
stratifies patients as follows:6 0) No evidence of
neuropathy, 1) neuropathy present but no evidence of
foot deformity or PVD, 2) neuropathy with evidence of
deformity or PVD, 3) history of foot ulceration or lower
extremity amputation. At least 2 of the following i.e.
erythema, warmth, tenderness or swelling should be
present to make a presumptive diagnosis of diabetic foot
infection. Osteomyelitis is likely to be present if bone can
be seen at the floor of deep ulcer.7 Aerobic gram-positive
cocci which include Staphylococcus aureus (S. aureus),
Streptococcus agalactiae (S. agalactiae), Streptococcus
pyogenes (S. pyogenes) and coagulase negative
staphylococci are mostly responsible for superficial
diabetic foot infections (cellulitis and infected ulcers in
antibiotic-naive patients).8
Deep and chronically infected ulcers and those that are
previously treated with antibiotics, are more likely to be
polymicrobial and in addition to above mentioned
microorganisms; involve Enterococci, Enterobacteriaceae,
Pseudomonas aeruginosa (P. aeruginosa), and
anaerobes.8 Wounds with extensive local inflammation,
necrosis, malodorous drainage, necrosis, or gangrene
with signs of systemic toxicity should be presumed to
have anaerobic organisms in addition to the above
pathogens.8 Microbiological spectrum also differs by
geographic location; with gram-negative pathogens
predominating in the sub-tropical climates of Africa and
Asia, in contrast to gram-positive organisms in the
western parts of the world.9 Current study is aimed at
identifying the common pathogens involved in diabetic
foot infections in our set-up and their susceptibility to
commonly used antimicrobial therapy that may guide in
selection of effective empiric treatment.
M a t e r i a l a n d Me thods
This was a cross sectional study, conducted in the
Department of Surgery, Pakistan Institute of Medical
Sciences (PIMS), Islamabad. Duration of study was one
year, from January 2017 to December 2017. Patients,
presenting in the outpatient department, emergency or
ward, qualifying the criteria of PEDIS (Perfusion, Extent,
Depth, Infection and Sensation) system of diabetic foot
classification were included in the study.10 This study was
approved by the ethics committee of the hospital and
written informed consent was obtained from all the
patients prior to enrolment in this study. A total of 118
patients presenting with signs and symptoms suggestive
of Diabetic Foot Infection were included in this study
through consecutive sampling technique.
Sample size was calculated through WHO sample size
calculator by using 95% confidence interval, 80% power
of study and 7.4% prevalence of diabetic foot ulcer in
Pakistan.11 Calculated sample size was 106 diabetic
patients. In order to overcome the possibility of dropouts,
total 118 patients were included in the study. Collected
samples included swabs, pus and tissue material after
cleansing with non-antimicrobial substance. At the time of
sample collection, no patient was on antimicrobial
therapy. Samples were sent promptly to microbiology
laboratory where they were cultured on blood agar and
MacConkey agar plates. Organisms were further
identified using respective biochemical tests according to
standard microbiological protocols. Bacteria that were
cultured included S. aureus, E. coli, P. aeruginosa,
Proteus, Klebsiella pneumoniae, methicillin resistant S.
aureus, Staphylococcus epidermidis, Acinetobacter, S.
viridans and Enterobacter. A Polymicrobial group was
added when culture was positive for two or more
J Islamabad Med Dental Coll 2019
10
organisms. Isolates were tested for susceptibility to
commonly used antimicrobial therapy. Antibiotics that
were included in culture sensitivity included
Piperacillin/Tazobactam, Linezolid, Ceftriaxone,
Vancomycin, Imipenem, Meropenem, Levofloxacin, Co-
Amoxiclav, Cefoperazone /Sulbactam, Amikacin,
Clindamycin, Ceftazidime, Ciprofloxacin, Tigecycline,
Chloremphenicol, Tobramycin and Cefoxitin. Statistical
Package for Social Sciences (SPSS) version 22 was used
to analyze data. The categorical data is presented in
frequencies and percentages i.e. gender frequency, most
common organisms and most sensitive antibiotics.
R e s u l t s
A total of 118 patients were included in this study with a
mean age of 53 ± 9.8 years. Out of 118 patients, 85 were
males (72%), and 33 were females (28%). About 105
patients (89%) tested positive for bacterial growth, while
13 patients (11%) had no organism growth on culture. Of
the culture positive patients, 71.4% were males and
28.6% were females. Cultured organisms were divided
into 11 groups. First five organisms isolated in 105 culture
positive patients in descending order were, S. aureus
(32.4%; n=34), E. coli (17.1%; n=18), P. aeruginosa
(14.3%; n=15), Polymicrobial (14.3%; n=15) and K.
pneumoniae (7.6%; n=8) (Table I). Top five antibiotics to
which organisms were sensitive in descending order were
Piperacillin/Tazobactam (69.5%), Imipenem (55.2%),
Amikacin (43.8%), Vancomycin (40%) and Levofloxacin
(38.1%) (Table II).
Table I: Frequency and Percentage of organisms isolated in
culture positive patients (n=105)
Sr.
No
Organism
Frequency
Percentage
1
Staphylococcus aureus
34
32.4%
2
Escherchia coli
18
17.1%
3
Pseudomonas aeruginosa
15
14.3%
4
Polymicrobial
15
14.3%
5
Klebsiella pneumoniae
8
7.6%
6
Proteus
5
4.8%
7
Methicillin resistant
staphylococcus aureus
3
2.9%
8
Staphylococcus epidermidis
3
2.9%
9
Acinitobacter
2
1.9%
10
Streptococcus viridans
1
1%
11
Enterobacter
1
1%
On an individual basis, S. aureus (n=34) was most
sensitive to vancomycin (61.8%; n=21), E. coli (n=18) was
most sensitive to Piperacillin/Tazobactam (88.9%; n=16),
P. aeruginosa (n=15) was most sensitive to
Piperacillin/Tazobactam (100%; n=15), Polymicrobial
(n=15) was most sensitive to Piperacillin/Tazobactam and
Amikacin (60%; n=9) and K. pneumoniae (n=8) was most
sensitive to Piperacillin/Tazobactam (75%; n=6) (Table
III).
Table II: Frequency and Percentage of antibiotic sensitivity
against organisms isolated (n=105)
Sr No
Antibiotic
Frequency
Percentage
1
Piperacillin/Tazobactam
73
69.5%
2
Imipenem
58
55.2%
3
Amikacin
46
43.8%
4
Vancomycin
42
40%
5
Levoflaxacin
40
38.1%
6
Cefoperazone/Sulbactam
34
32.4%
7
Co-amoxiclav
33
31.4%
8
Ceftriaxone
22
21%
9
Linezolid
16
15.3%
10
Meropenem
16
15.3%
11
Tobramycin
13
12.4%
12
Ciprofloxacin
6
5.7%
13
Tigecycline
5
4.8%
14
Clindamycin
4
3.8%
15
Chloremphenicol
4
3.8%
16
Ceftazidime
2
1.8%
17
Cefoxitin
1
1%
D i s c u s si on
Our study shows that there is a male predominance in
patients of diabetic foot with male to female ratio of 2.5:1.
Other studies carried out in Pakistan either show higher
male predominance of 4:1 for diabetic patients at Nishtar
Hospital, Multan 12 and CMH Peshawar,13 or comparable
ratio of 2.3:1.14 Male predominance can be due to males
working outdoors exposed to contaminated surroundings
compared to females performing household chores.
Moreover, females in general are more concerned about
their health and adopt preventive strategies. Our study
shows mean age of 53 ± 9.8 years, which is in agreement
to a study done on 73 patients in Karachi with a mean
age of 52.7 ± 9.4 years.15 According to another study
carried out in Nishtar Hospital Multan, the most commonly
affected age group was also 50 to 60 years.12 The logical
explanation for affecting older individuals is that Diabetes
is usually diagnosed at a later age with multiple
J Islamabad Med Dental Coll 2019
11
Table III: Top five common organisms and their sensitivity to different antibiotics
Sr
No
Antibiotic Sensitivity
S. Aureus
(n=34)
E. Coli
(n=18)
Pseudomonas
(n=15)
Polymicrobial
(n=15)
Klebsiella
(n=8)
1
Piperacillin/ Tazobactam
55.9% (n=19)
88.9% (n=16)
100% (n=15)
60% (n=9)
75% (n=6)
2
Imipenem
52.9% (n=18)
66.7% (n=12)
80% (n=12)
40% (n=6)
37.5% (n=3)
3
Amikacin
26.5% (n=9)
44.4% (n=8)
40% (n=6)
60% (n=9)
75% (n=6)
4
Vancomycin
61.8% (n=21)
22.2% (n=4)
33.3% (n=5)
26.7% (n=4)
12.5% (n=1)
5
Levoflaxacin
50% (n=17)
27.8% (n=5)
46.7% (n=7)
6.7% (n=1)
12.5% (n=1)
co-morbidities, poor diabetic control and nutritional
deficiencies. The most common groups of organisms
identified in this study are S. aureus, E. coli, P.
Aeruginosa and Polymicrobial. This was also seen in a
study done in Khyber Pakhtunkhwa where S. aureus and
E. coli were the most common organisms in diabetic foot
patients.16 In another study Staphylococcus aureus was
the most prevalent organism constituting 23.16% of the
organisms isolated followed by Escherichia coli (17.89%)
and Klebsiella (12.63%).15 Proteus, S. aureus, Klebsiella
and P. aeruginosa were the most widely recognized
microorganisms of diabetic foot infections.17 Another
study showed S. aureus being the most commonly
isolated organism.18,19 Our findings are comparable with
other studies conducted in this region. In our study,
organisms are most sensitive to Piperacillin/Tazobactam,
Imipenem, Amikacin, Vancomycin and Levofloxacin. In a
study on diabetic foot ulcers in Jinnah Postgraduate
Medical Center, Karachi organisms were most sensitive to
Meropenem, effective in 95% patients.15
The specific antibiotic given against culture sensitive
organisms helps in prevention of drug resistance, more
accurate management and speedy recovery rather than
empirical therapy. So, each organism being more
sensitive to specific antibiotic should be treated with
antibiotic of choice accordingly. Culture sensitivity should
be done regularly to identify the organism and start proper
antibiotic regimen. Hospital based studies can also help in
maintaining an antibiogram, which should be periodically
updated for devising antibiotic protocols for effective
treatment of bacterial infections.
C o n c l us i on
Diabetic foot infections are common in older age group
with male predominance. Most common infecting
organisms included S. aureus, E. coli, P. aeruginosa,
Polymicrobial and Klebsiella with Piperacillin/
Tazobactam, Imepenem, Amikacin, Vancomycin and
Levofloxacin emerging as the most sensitive antibiotics in
our diabetic patients.
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