Microbial Pattern of Diabetic Foot Ulcer Patient in Jemursari

Islamic Hospital Surabaya Period 2012–2016

Adyan Donastin1, Aisyah1

1
Department of Medicine, Faculty Abstract
of Medicine, Nahdlatul Ulama
University of Surabaya, Surabaya, Diabetic foot ulcers (DFU) are complications in people with
Indonesia diabetes mellitus (DM) in the form of wounds or tissue
damage resulting in vascular insufficiency and or
neuropathy that can develop into an infection. Early
Correspondence:
detection of germs of diabetic foot ulcers may be used as a
Aisyah, Jl. Jemursari No. 51-57,
recommendation of empirical therapy before the definitive
Surabaya, East Java, Indonesia
Zip Code : 60237
treatment based on culture results and appropriate
antibiotics treatment, which may reduce hospitalization time
Email: [email protected] and amputation events. According to Riskesdas in 2013,
state that the number of antibiotic used without prescriptions
Received: February 26, 2019 in Indonesia about 86.1%. The study aims to retrospectively
Revised: March 26, 2019 analyze the bacterial culture and drug susceptibility test
Accepted: April 1, 2019 results for patients with diabetic foot ulcers (DFU) in
Jemursari Islamic Hospital Surabaya during 2012–2016 to
help clinicians choose a more appropriate empirical
antibiotic treatment for DFU. This study used cross–
sectional designed with retrospective approaches, which
analyzed descriptively and samples were taken by the total
sampling of 11 samples. This research was conducted at
Islamic Hospital of Jemursari Surabaya in May–September
2017 by using medical record data which are outpatient and
inpatients who treatment at Jemursari Islamic Hospital. The
result was found 6 types of bacteria consisting of
Staphylococcus aureus (18%), Staphylococcus non–
haemolytic (18%), Klebsiella pneumonia (27%),
Enterobacter aerogenes (18%), Burkholderia cepacia (9%),
Escheria coli (9%). The most sensitive antibiotics in the
Gram–positive bacteria in this study are Amikacin,
Teicoplanin and Oxacillin and the most resistant to
Amoxicillin and Ampicillin whereas the most sensitive
antibiotics in the Gram–negative bacteria in this study were
Meropenem and the most resistant to Ciprofloxacin and
Trimethroprim–sulfamethoxazole.

Keywords
Microbial pattern, antibiotics sensitivity pattern, diabetic,
foot ulcer, diabetes mellitus

22
 Adyan Donastin, Aisyah

INTRODUCTION patients with DM compared with non–DM

Diabetes Mellitus (DM) is one of the (8), and about 85% amputation in DM

main problems in public health system that patients associated with DFU (9), can even

has increased dramatically over the past 2 end in disability or death (10). The current

decades and continues to increase (1–3). DFU prevalence in Indonesia is 12%, while

Based on research by the World Health the prevalence of DFU risk factors in

Organization (WHO) in developing countries Indonesia is 55.4% (11).

showing the highest increase in DM patients Several studies show that there are

in Southeast Asia including Indonesia and it variations in the types of germs that cause

is estimated that in the next 1 or 2 decades the DFU, both aerobic and anaerobic germs.

frequency of DM in Indonesia will increase Akbar et al. (29) in Arifin Achmad Hospital

dramatically to rank number 5 in the world for 23 samples received A. baumanii

(4). Diabetes mellitus that is not treated (34.8%), K. pneumoniae (26.2%), E. coli

properly will cause complications, as is the (17.4%), E. cloacae (8.7%), P. stuartii

most common and often occurs is diabetic (4.3%), R. ornithinolytica (4.3%), and P.

foot ulcer (DFU). Damage will arise if in the aeruginosa (4.3%). Research by Akhi et al.

long term there is a decrease in blood flow (2015) of 60 samples obtained S. aureus

accompanied by nerve damage (neuropathy) (28%), Enterobacteriaceae (24%), E. coli

in the legs, thereby increasing the likelihood (15%), Citrobacter spp. (4%), Enterobacter

of DFU. spp. (4%), and Staphylococcus spp. negative

Diabetic foot ulcer is a wound that occurs coagulase (17%), Enterococcus spp. (15%),

in the legs of people with type 1 diabetes and P. aeruginosa (7%), Acinetobacter spp.

2, then infection and or tissue damage (4%), and Bacteroides fragilis (4%).

resulting from neuropathy (nerve disorders), Data from previous studies show that

angiopathy (impaired blood flow in the legs) early detection of germs in DFU can be used

or both that often become the place of entry as a recommendation for empirical therapy

of bacteria into the legs (5–6). Gardner (7) before definitive therapy based on the results

states that around 15% of patients suffering of culture and appropriate antibiotics, so as to

from DM will develop into DFU during their reduce the time of hospitalization and the

lifetime (7). Further infections without good incidence of amputation. The results of

treatment and adequate can be the most Riskesdas in 2013 also stated that the use of

common cause of amputation, and based on prescription antibiotics in Indonesia was

non–traumatic events with the risk of 86.1%. This study aims to retrospectively
23

amputation 10–20 times more often in analyze the bacterial culture and drug

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 Adyan Donastin, Aisyah

susceptibility test results for patients with a cross–sectional design with a retrospective
diabetic foot ulcers (DFU) in Jemursari approach. Evaluate the results of medical
Islamic Hospital Surabaya during 2012–2016 records regarding germs that cause DFU and
to help clinicians choose a more appropriate the rational use of antibiotics in these cases.
empirical antibiotic treatment for DFU.
RESULTS
MATERIALS AND METHODS DFU patients who were hospitalized at

The data collected are secondary data Jemursari Hospital from 2012 to 2016 totaled

based on research variables taken from the 291 patients. Data on DFU patients were then

Clinical Pathology Laboratory Installation of compared with data on patients who

Jemursari Surabaya Islamic Hospital for the underwent pus culture at Jemursari Hospital.

2012–2016 periods. The population in this The data of the patients taken were 57 data on

study was medical records of patients with DFU patients with a history of undergoing a

diabetes mellitus with complications of specimens culture of pus at Jemursari

diabetic foot ulcers at Jemursari Islamic Hospital. The inclusion criteria in this study

Hospital Surabaya in January 2012– were medical records of DM patients with

December 2016. The samples in this study DFU who were hospitalized at Jemursari

were medical records of patients with Hospital with a complete identity, results of

diabetes mellitus with complications of pus culture test, and antibiotic sensitivity test.

diabetic foot ulcers in January 2012– Based on the inclusion criteria of this study,

December 2016, which fulfills the inclusion 46 patient data were excluded from the study

and exclusion criteria, and samples are taken because there were no forms of pus culture

in total sampling. The inclusion criteria in test results and antibiotic sensitivity tests

this study were medical records of DM from the laboratory, so that the samples used

patients with DFU who are hospitalized at in this study were 11 patients.

Jemursari Hospital with complete identity, Distribution of DFU patients according

results of pus culture test, and antibiotic age and sex

sensitivity test and exclusion criteria were Table 1 showed that the results are

grade 0 and grade 1 ulcers. differentiated by age group (16), with the age

This research was carried out group 1–12 years and 12–18 years there are

descriptively because the observations were no DFU patients, in the age group 18–60

carried out according to the conditions as years, 195 patients (67.01%), and at age> 60

they were without any direct treatment from years there were 96 patients (32.99%), with
24

the researchers on the test subjects and using an average age of 55.55 years. In this study,

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 Adyan Donastin, Aisyah

there were 152 male patients (52.23%), while Distribution of pathogenic germs to pus
139 female patients (47.77%). specimens
The results of germ culture from pus
Table 1. Distibution of DFU patients specimens in DFU patients at Jemursari
according age and sex
Hospital showed in Figure 1. It showed that
Percentage
Patient Freq. the 11 germ samples obtained two types of
(%)
Age 1–12 years old 0 0
germs, namely Gram–positive and Gram–
> 12–18 years old 0 0
negative germs. The Gram–positive germs
> 18–60 years old 195 67.01
>60 years old 96 32.99 found in this study were Staphylococcus non-
Sex Man 152 52.23
haemolyticus and Staphylococcus aureus,
Woman 139 47.77
while the Gram–negative germs found in this
study were Escherichia coli, Enterobacter
aerogenes, Burkholderia cepacia, and
Klebsiella pneumonia.

Fig 1. Distribution of pathogenic germs to pus specimens

The sensitivity pattern of Gram–positive the antibiotics most resistant to Gram–

germs to some antibiotics positive germs were Amoxycilin and
The most sensitive antibiotics used in Ampicillin.
Gram–positive germs in this study were
Amikacin, Teicoplanin, and Oxacilin, while
25

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 Adyan Donastin, Aisyah

Percentage of sentivity

Fig 2. The sensitivity pattern of Gram–positive germs to some antibiosis

Percentage of sentivity

Fig 3. The sensitivity pattern of non haemolytic Staphylococcus antibiotics

The sensitivity pattern of Gram–negative Meropenem, while the antibiotic most

germs to some antibiotics resistant to Gram–negative germs is
The most sensitive antibiotic used in Ciprofloxacin and Trimethroprim–
26

Gram–negative bacteria in this study is sulfamethoxazole.

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 Adyan Donastin, Aisyah

Percentage of sentivity

Fig 4. The sensitivity pattern of the antibiotic Klebsiella pneumonia

Percentage of sentivity

Fig 5. The sensitivity pattern of the antibiotic Enterobacter aerogenes

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 Adyan Donastin, Aisyah

Percentage of sentivity

Fig 6. The sensitivity pattern of Escherichia coli antibiotics

Percentage of sentivity

Fig 7. The pattern of antibiotic sensitivity of Burkholderia cepacia

DISCUSSION RSUP dr. M Djamil Padang in 2007, which

Distribution of DFU patients according obtained the highest age group, was 40–59

age and sex years as many 65.8% (13–14). The age of

The distribution of the age groups of patients suffering from diabetes and age at

patients with the most DFU in this study was complications (one of them is diabetic ulcers)

18–60 years as many as 195 (67.01%) with is related, this is in accordance with Tarigan's

an average age of 55.55 years. Old age is one study at Herna Hospital in Medan in 2009–

of the factors that influence DM, which can 2010 where the highest DM patients in the

cause neuropathy complications in patients age group >40 years as DM age groups the
28

with DFU (12). The results of this study are most is 128 (95.5%) (15).

in accordance with Decroli’s research in

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 Adyan Donastin, Aisyah

Based on these studies it can be men (71%) in RSUP Dr. M. Djamil Padang,
concluded that the age group with the most and in accordance with the Gaol study (19),
DFU is in the productive age group to old which gets the sex distribution more
age. This could be attributed to people's dominant in men (54%) in Dr. RSUP M.
lifestyles and eating patterns, especially those Djamil Padang in 2011–2013 (19). This study
that are not good (16). Based on the results of was also in accordance with Commons
the Basic Health Research (Riskesdas) in research at the Royal Darwin Hospital in
2007, it was found that the proportion of 2015 with data on 177 patients found to be
deaths due to diabetes mellitus in the 45–54 predominantly male (60%) (20). The
year age group in urban areas was ranked research conducted by Danmusa (21)
second, namely 14.7% and national explained that the incidence of DFU was
prevalence of DM based on examination of more prevalent in men (67.2%) compared to
population gaet >15 years in urban areas is women (32.8%). This study also According
5.7%. This illustrates that DM disease, to Chomi et al. (22) Diabetic ulcer
especially in urban areas are serious and distribution in men can be caused by men
impactful problem productive age group compared with women who consult doctors
productivity (17). Diabetic ulcer often occurs less often, and information given to doctors
at the age of >50 years due to decreased tends to be less (22). The research conducted
physiological body functions such as by Danmusa (21) explained that the incidence
decreased insulin secretion or resistance, so of DFU was more prevalent in men (67.2%)
that the ability of the body to function on high compared to women (32.8%). Jobs for men
blood glucose control is less optimal. spend more time outdoors and do more work
Uncontrolled blood sugar levels will result in severe, making it easier for DFU to occur and
long chronic complications, both macro– and increasing the risk of amputation.
micro vascular, one of which is diabetic ulcer Amputation in male DM patients has twice
(18). the risk (22–23).
Factors that influence DM complications This research is not in line with Fahmi's
and are related to DFU other than age are (24) research in Cengkareng Regional
gender. In this study, it was found that DFU General Hospital in 2013–2014 where
patients in Jemursari Hospital were more women were dominant (57.6%), and
prevalent in men (52.23%) than women Witanto's research at Immanuel Hospital in
(47.77%). This study is in line with the Bandung, which had more dominant female
research of Decroli (2008) who obtained a distribution (63%) (24–25).
29

sex distribution that was more dominant in

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 Adyan Donastin, Aisyah

The difference in research between the Cefepime, Cefoxitin, Levofloxacin,

two groups can be overcome if this research Trimethroprim–sulfamethoxazole, and
is conducted with more and more Erythromycin. S. aureus was found to be
representative sample sizes. 100% resistant to Ofloxacin, Vancomycin,
Distribution of Gram–positive and Gram– Amoxycilin, and Ampicillin, 50% resistant to
negative germs Amoxicilin–clavulanic acid, Piperacillin–
Based on this study and other studies it tazobactam, Meropenem, Cefepime,
can be seen that germs found in DFU patients Cefoxitin, Levofloxacin, and
at different places and at different times not Trimethroprim–sulfamethoxazole.
exactly the same, but some of the same germs Infection patients who are given
like S. aureus, K. pneumoniae, E. coli and penicillin as the first therapy and their
Enterobacter are obtained. The Gram– incomplete administration can cause
positive germs that were present in the DFU resistance since the emergence of
in this study were S. aureus (18%) and non methicillin–resistant S. aureus, vancomycin
haemolytic Staphylococcus (18%). Gram– glycopeptide is the only uniformly effective
negative germs present in DFU in this study treatment for Staphylococcus infection.
were K. pneumoniae (27%), E. aerogenes Resistance of vancomycin glycopeptide to S.
(18%), B. cepacia (9%), E. coli (9%). In this aureus (27). This study is in accordance with
study, it was found that infection in DFU was the research of Chaudhry et al. (28) who
still caused by a polymicrobial infection so received Staphylococcus aureus were
that the pattern of diabetic foot infection resistant to Penicillin (100%), Vancomycin
specifically could not be ascertained. Each (80%), and Ampicillin (30%) (28).
study has different characteristics of germ The sensitivity pattern of Gram–negative
patterns depending on the patient's condition germs to some antibiotics
and environment so different empirical K. pneumoniae was found to be most
antibiotic therapies are needed as well (26) sensitive to Amikacin, Gentamycin,
The sensitivity pattern of Gram–positive Amoxicilin–clavulanic acid, Cefoperacilin
germs to some antibiotics sulbactam, Piperacilin–tazobactam,
S. aureus was found to be 100% sensitive Meropenem, and Ceftrizoxime. K.
to antibiotics Amikacin, Ceftriaxone, pneumonia was found to be 100% resistant to
Teicoplanin, Clindamycin, Azithromycin, the antibiotic moxifloxacin fluoroquinolone,
Linezolid, Oxacilin, and Chloramphenicol, resistant 66.67% of Ciprofloxacin,
50% sensitive to Amoxicilin–clavulanic acid, Levofloxacin, Ofloxacin, Trimethroprim–
30

Piperacillin–tazobactam, Meropenem, sulfamethoxazole, and Chloramphenicol,

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 Adyan Donastin, Aisyah

while 50% were resistant to Cefepime, (18%), B. cepacia (9%), E. coli (9%) The
Cefotaxime, Ceftazidime, Ceftriaxone, and dominant germ found in diabetic foot ulcer
Aztreonam. patients at Jemursari HospitalI period 2012–
Akbar et al. (29) obtained K. pneumonia 2015 is a Gram–negative germ, namely K.
sensitive to Amikacin antibiotics (100%) pneumonia (27%). The sensitivity of
(29). This study is in accordance with the antibiotics to germs consist of the most
research of Chaudhry et al. (28) who received sensitive antibiotics in Gram–positive germs
K. pneumonia resistant to Ceftazidime in this study were Amikacin (100%),
(100%), Ceftriaxone (100%), Cefepime Teicoplanin (100%), and Oxacillin (100%),
(100%), Cefotaxime (80%), Aztreonam and the most resistant to Amoxicillin (0%)
(60%), and Chloramphenicol (20%) (28). and Ampicillin (0%). The most sensitive
antibiotic used in Gram–negative germs in

CONCLUSIONS this study is Meropenem (100%), while the

antibiotic most resistant to Gram–negative
In this research, it can be concluded that
germs is Ciprofloxacin (0%) and
the age group of patients with the most DFU
Trimethroprim–sulfamethoxazole (0%).
is the age group 18–60 years as many as 195
(67.01%) patients, with an average age of
55.55 years. Based on gender, the majority of CONFLICT OF INTEREST
DFU patients were men (152.23%). The There are no conflicts of interest.
germs found in this study were S. aureus
(18%), non–haemolytic Staphylococcus
(18%), K. pneumoniae (27%), E. aerogenes

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