Skip to main content
Top
Gepubliceerd in: Journal of Foot and Ankle Research 1/2020

Open Access 01-12-2020 | Research

Clinical and bacteriological profile of diabetic foot infections in a tertiary care

Auteurs: Teik Chiang Goh, Mohd Yazid Bajuri, Sivapathasundaram C. Nadarajah, Abdul Halim Abdul Rashid, Suhaila Baharuddin, Kamarul Syariza Zamri

Gepubliceerd in: Journal of Foot and Ankle Research | Uitgave 1/2020

share
DELEN

Deel dit onderdeel of sectie (kopieer de link)

  • Optie A:
    Klik op de rechtermuisknop op de link en selecteer de optie “linkadres kopiëren”
  • Optie B:
    Deel de link per e-mail
insite
ZOEKEN

Abstract

Background

Diabetic foot infection is a worldwide health problem is commonly encountered in daily practice. This study was conducted to identify the microbiological profile and antibiotic sensitivity patterns of causative agents identified from diabetic foot infections (DFIs). In addition, the assessment included probable risk factors contributing to infection of ulcers that harbour multidrug-resistant organisms (MDROs) and their outcomes.

Methods

We carried out a prospective analysis based on the DFI samples collected from 2016 till 2018. Specimens were cultured with optimal techniques in addition to antibiotic susceptibility based on recommendations from The Clinical and Laboratory Standards Institute (CLSI). A total of 1040 pathogens were isolated with an average of 1.9 pathogens per lesion in 550 patients who were identified with having DFIs during this interval.

Results

A higher percentage of Gram-negative pathogens (54%) were identified as compared with Gram-positive pathogens (33%) or anaerobes (12%). A total of 85% of the patients were found to have polymicrobial infections. Pseudomonas aeruginosa (19%), Staphylococcus aureus (11%) and Bacteroides species (8%) appeared to be the predominant organisms isolated. In the management of Gram-positive bacteria, the most efficacious treatment was seen with the use of Vancomycin, while Imipenem and Amikacin proved to be effective in the treatment of Gram-negative bacteria.

Conclusion

DFI’s are common among Malaysians with diabetes, with a majority of cases displaying polymicrobial aetiology with multi-drug resistant isolates. The data obtained from this study will be valuable in aiding future empirical treatment guidelines in the treatment of DFIs. This study investigated the microbiology of DFIs and their resistance to antibiotics in patients with DFIs that were managed at a Tertiary Care Centre in Malaysia.
Opmerkingen

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Afkortingen
DFIs
Diabetic foot infections
MDROs
Multidrug-resistant organisms
CLSI
Clinical and Laboratory Standards Institute
DM
Diabetes Mellitus
WHO
World Health Organization
ESBLs
Extended spectrum beta-lactamases
MRSA
Methicillin-resistant Staphylococcus aureus
HBOT
Hyperbaric Oxygen Therapy
BA
Blood agar
API
Analytical profile index
SPP
Species
IDSA
Infectious Diseases Society of America
IWGDF
International Working Group of Diabetic Foot

Background

A worrying global health predicament in the modern age is Diabetes Mellitus (DM). Approximately 150–170 million of the world’s population is suffering from this condition and its prevalence will most likely multiply by two folds by 2025 as per the World Health Organization (WHO) reports [1]. The WHO has identified the leading 10 countries in Asia with a large number of people with DM including India, Japan, China, Korea, Bangladesh, Thailand, Indonesia, Philippines and Malaysia. Malaysia is forecast to have an estimated leap from 2.5 million people with DM in the year 2018 to a drastic and frightening increase to 5 million people by the year 2030 [2]. The preponderance of DM in Malaysia is almost 32% of the population which has significantly increased from 0.6% in 1960 to 2.1% in 1982, 6.3% in 1986, 8.3% in 1996 and 14% in 1998 [3, 4]. DM is now estimated to affect the lives of 16–18% of Malaysians [3, 5]. Patients who do not have good control of their DM are at risk of developing complications arising from diabetes which are macrovascular and microvascular. Among these complications are neuropathy, retinopathy and pedal ulcers with or without gangrene [3]. Almost 15% of patients with DM eventually end up developing foot ulcers that can progress to osteomyelitis [6]. The progression of these wounds from superficial to debilitating infections are facilitated by impaired defence mechanisms of the body and delayed treatment. The subcutaneous tissue infections have the ability to spread to the deeper structures which will ultimately progress into complications including gangrenous changes and also amputations [7]. Poor control of DM puts a patient at higher risk of skin infections as being in a state of hyperglycaemia impairs the efficiency of the body’s immune or defence mechanism [8]. Diabetic foot infections (DFIs) are complex, rampant and costly ramifications of DM. These infections account for the majority of DM related hospitalisations other than non-traumatic amputations [9]. Few have studied the relationship between number of organisms identified and the types of infections that occur from it. In 2003, Frykberg concluded that most mild infections are commonly monomicrobial in which Gram-positive cocci such as Streptococcus species and Staphylococcus aureus were identified.
Contrarily, the more severe forms of DFI’s are commonly polymicrobial in which the causative organism include Gram-negative bacilli (e.g., Klebsiella species., Proteus species., Escherichia coli, Pseudomonas species.) aerobic Gram-positive cocci, and anaerobes [10].
Prompt initiation of ideal therapy for DFIs plays a role in the reduction of morbidities interlinked with infections. Despite that, there can be a reduction in the number of hospitalisations and their durations in addition to reducing the incidence of major limb amputation. There are many factors that contribute to successful clinical outcomes, which include prompt lesion recognition followed by host factor modification, expeditious commencement of ideal antibiotic therapy plus efficient surgical intervention which includes debridement of bone and soft necrotic tissue. Prompt antibiotic therapy should be initiated to improve limb saving probabilities as many DFIs are true emergencies [11]. The aim of this study was to further enhance understanding on the bacteriology of diabetic foot ulcers alongside the assessment of the in vitro antimicrobial susceptibility of the offending pathogens in the General Hospital of Melaka, which is located in the historical state of Melaka, Malaysia and Universiti Kebangsaan Malaysia Medical Centre which is located in central Kuala Lumpur, both with a capacity to accommodate nearly one thousand patients. These two hospitals are major general tertiary care centres in their respective states and are the primary centres that receive referrals for further management of DFI’s.

Materials and methods

This prospective study included 550 patients with longstanding and newly diagnosed DM who presented with lower extremity infections requiring admission to the General Hospital of Melaka and Universiti Kebangsaan Malaysia Medical Centre. This study was conducted over a period of 2 years between 1st February 2016 and 1st February 2018. There was no duplications in the recruitment of patients in the study. Patients underwent clinical assessment and proper grading of their foot lesions was carried out in accordance with the DFI severity classification systems including the Wagner Classification System and the University of Texas Wound Classification System [12]. The classifications of wounds were according to the severity which was mild, moderate or severe based on the size, depth and level of the tissue involved in the infection, presence of metabolic instability or any systemic manifestations of infection. Briefings were given to patients regarding the details of the study. Patient information including age, gender, type of diabetes and duration of DFI’s were recorded. Various specimens (wound exudates, pus or tissue biopsy) from the ulcerated regions were collected for microbiological studies. The surface of those regions was thoroughly rinsed with sterile normal saline solution and pus samples were taken using sterile cotton swabs. A total of 550 patients were identified from request forms and their clinical specimens were subsequently dispatched to the microbiology laboratory for further analysis. The forms were designed to provide pertinent demographic data and clinical information including a patient’s age, gender, race, nature of the specimen, examination required, diagnosis and details of antimicrobial therapy. The request forms were completed and signed by the respective treating medical officers. Data were recorded according to patient’s age, gender, ethnicity alongside nature of the clinical specimen, species of the isolated pathogen and antibiogram of the clinical isolates.

Wagner’s classification of diabetic foot ulcers

Grade 0: no ulcer in a high-risk foot.
Grade 1: superficial ulcer involving the full skin thickness but not underlying tissues.
Grade 2: deep ulcer, penetrating down to ligaments and muscles, but no bone involvement or abscess formation.
Grade 3: deep ulcer with cellulitis or abscess formation, often with osteomyelitis.
Grade 4: localized gangrene.
Grade 5: extensive gangrene involving the whole foot.

University of Texas Wound Classification System of diabetic foot ulcers

Grade IA: not infected, no ischemic superficial ulceration.
Grade IB: infected, no ischemic superficial ulceration.
Grade IC: ischemic, no infected superficial ulceration.
Grade ID: ischemic, infected superficial ulceration.
Grade IIA: not infected, no ischemic ulcer that penetrates to capsule or bone.
Grade IIB: infected, no ischemic ulcer that penetrates to capsule or bone.
Grade IIC: ischemic, no infected ulcer that penetrates to capsule or bone.
Laboratory investigations and hospital records of patients recruited into the study between February 2016 to February 2018 were reviewed meticulously. The technique of specimen collection included clinically infected wounds while excluding superficial or colonizing organisms. Specimen isolates were not duplicated in this study. The specimen cultures were obtained once the wound surface had been irrigated with copious normal saline, and we subsequently debrided the superficial tissue and separated them from the exudates to isolate the colonizing pathogenic flora. Specimens were obtained by curetting the ulcer base post debridement and by aspirating the infected skin or deep tissues. The specimens underwent gram staining and inoculation on both selective and non-selective media including MacConkey agar (Oxoid), blood agar (BA; Oxoid, Basingstoke, UK), chocolate agar and 5% (v/v) BA supplemented with vitamin K1 (1 μg/ml), gentamicin (75 μg/ml) (GBA) and haemin (5 μg/ml). The inoculated plates were incubated under conducive atmospheric conditions for 24–48 h to enable bacterial isolation. Isolated organisms were identified by traditional microbiological methods: Analytical profile index 20 (API 20) Strep for streptococci and enterococci, API 20A (bioMérieux, Marcy l’Etoile, France) and GLC (Chromopak, CP9001, The Netherlands) for anaerobes, API 20E for Gram-negative aerobes and API Staph for staphylococci. According to the standardised procedures described by Sharma, the bacteria were isolated and classified by microscopy, morphology and biochemical testing [13].

Antimicrobial susceptibility testing

In accordance with the guidelines of the Clinical and Laboratory Standards Institute (CLSI), confirmation of antimicrobial susceptibility of the bacterial isolates was carried out by using the disk diffusion method [14]. Isolated bacterial colonies were suspended in sterile distilled water and matched to the 0.5 McFarland standard [5, 15]. A sterile swab was soaked into the inoculums and subsequently used to streak the Mueller–Hinton agar plates for Gram-negative bacilli, Staphylococci, and Enterococci. For Streptococci, the Mueller–Hinton agar was supplemented with 5% horse blood as described in the CLSI guidelines and followed by application of antibiotic discs on the plates. The inoculated agar plates were incubated at 35–37 °C for 18–20 h. Then, the diameter of the inhibition zone was interpreted based on the guideline suggested by the CLSI. Staphylococcus aureus was tested for Methicillin resistance using a 1 μg Oxacillin disc. Reference strains of Escherichia coli and Pseudomonas aeruginosa were used as a control for Gram-negative bacteria and were included in the tests. Staphylococcus aureus and Enterococcus faecalis were used as Gram-positive control strains [14].

Results

Demographic characteristics

All 550 patients successfully recruited into the study were recruited. All had been diagnosed with Diabetic Foot Ulcer to participate in this particular study. The data of these patients were compiled and summarized in Table 1. In this study, 337 out of 550 (61%) were male and 213 out of 550 (39%) were female with a male-to-female ratio of 1.58:1. The patients’ age ranged from 37 to 91 years old with a mean of 56.7 years. Out of the total population, only 10 (1.8%) patients presented with type 1 DM and the rest 540 (98.2%) were type 2 DM. The majority of patients were Malaysian nationals 544 (98.9%). Indians and Malays accounted for 40% (n = 220) and 39% (n = 214) respectively, while the Chinese population accounted for 20% (n = 110) followed by 1% (n = 6) of the others.
Table 1
Demographic distribution of 550 patients with diabetic foot infections
Age (years)
Malaysian (n = 544)
Non-Malaysian (n = 6)
Total no. (%) (n = 550)
M
F
M
F
40≤
27
26
0
1
54 (9.8)
41–50
65
46
3
2
116 (21)
51–60
137
55
0
0
192 (35)
61–70
85
67
0
0
152 (27.6)
71–80
18
15
0
0
33 (6)
81–90
2
0
0
0
2 (0.4)
≥91
0
1
0
0
1 (0.2)
Total
334
210
3
3
550 (100)

Microbiology

From 550 patients, we were able to isolate 1040 pathogens averaging at 1.8 per lesion. We included the specimens with clinically significant pathogens which were wound tissue (220; 40%), swabs (220; 40%), pus (83; 15%) and bone (27; 5%). Patients were graded based on foot lesions and the number of bacterial isolates. Their numbers are shown in Table 2. Table 3 presents the multiple organisms isolated from the DFIs. 54% of aerobic gram-negative bacteria were isolated and it was the most commonly isolated pathogens. The four most common microbial isolates were Pseudomonas aeruginosa (19%), Staphylococcus aureus (11%), Methicillin-resistant Staphylococcus aureus (8%) and Bacteroides species (spp.) (8%).
Table 2
The number of patients in each grade of diabetic foot infection and the total number of bacteria isolated from different grades of diabetic foot infection
Grades of diabetic foot infection
No. of patients
A positive culture for bacteria
1
2
> 2
Mild
203
30
51
122
Moderate
227
34
57
136
Severe
120
18
30
72
Total
550
82
(15%)
138
(25%)
330
(60%)
Table 3
The proportion and frequency of microbial isolation from the samples
Bacteria
Total number
Proportion
Frequency
N = 1040
Gram-positive bacteria
348
33
63
Staphylococcus aureus
116
11
21
Methicillin-resistantS. aureus
86
8
15
Enterococcus spp.
63
6
11
Group B streptococci
47
4
9
Other streptococci
27
3
5
Other Staphylococcus spp.
9
1
2
Gram-negative bacteria
558
54
100
Pseudomonas aeruginosa
192
19
35
Proteus mirabilis
74
7
13
Klebsiella pneumonia
71
7
13
Enterobacter spp.
69
6
12
Escherichia coli
60
6
10
Non-fermenters
29
3
5
Morgenella spp.
20
2
4
Other Gram-negative
16
2
3
Serratia marcescens
15
1
3
Citrobacter spp.
12
1
2
Anaerobes
123
12
22
Bacteroides spp.
84
8
15
Anaerobic Streptococci
18
2
3
Microaerop Streptococci
10
1
2
Candida spp.
9
1
2
Clostridium spp.
6
0.5
1
Fusobacterium spp.
5
0.5
1
Proportion = the percentage of isolates organism divided into the total number of isolated organisms.
Frequency = the percentage of the organisms divided into the total number of patients.

Antibiotic susceptibility

Analysis of this study showed that 468 (85%) of the 550 infected patients had multiple microorganism infections. The most common microbial isolates in Gram-positive bacteria were Staphylococcus aureus (11%), Gram-negative bacteria was Pseudomonas aeruginosa (19%) and Anaerobes was Bacteroides species (8%) respectively.
Table 4 illustrates the antimicrobial susceptibility pattern of the Gram-positive cocci. Out of the 150 Staphylococcus aureus isolates, 94.8, 62.0, and 56% were penicillin-resistant, tetracycline and erythromycin, respectively. Vancomycin, the most sensitive antibiotic for Staphylococcus aureus organism. The Enterococcus spp. were susceptible to vancomycin and tetracycline, however, 63.5 and 15.9% were resistant to erythromycin and penicillin, respectively. The Group B Streptococcus isolates were susceptible to co-amoxiclav, penicillin, and ampicillin, but 51% were resistant to tetracycline. Table 5 demonstrates the pattern of antibiotic resistance for Gram-negative bacilli. Imipenem and Amikacin were the most active antimicrobial agents tested against all of the microbial isolates. Pseudomonas aeruginosa resistant towards Ciprofloxacin and Piperacillin-Tazobactam, both 18% resistance. As for Proteus species and Klebsiella pneumonia, both were highly resistant towards Ampicillin (45% & 79% respectively). The antibiotic susceptibility pattern of isolated anaerobes is shown in Table 6. Amoxicillin, Ampicillin, Cefoxitin, Metronidazole and Piperacillin/Tazobactam showed excellent sensitivity against all anaerobes; there were no resistance towards these antibiotics. Nonetheless, 67% of the anaerobic streptococci and 32% of the Bacteroides species were resistant towards clindamycin.
Table 4
Resistance pattern for most common Gram-positive cocci towards antimicrobials
Antimicrobial agents
Gram-positive organisms (% resistant)
S. aureus
Enterococcus spp.
Group B Streptococcus
n = 116
(%)
n = 63
(%)
n = 47
(%)
Ampicillin
59
50.8
0
0.0
Clindamycin
56
48.2
5
10.6
Cloxacillin
60
51.7
Co-amoxiclav
59
50.8
0
0.0
Erythromycin
65
56.0
40
63.5
8
17.0
Fusidic acid
60
51.7
Gentamicin
52
44.8
1
1.6
2
4.3
Penicillin
110
94.8
10
15.9
0
0.0
Rifampicin
1
0.8
Sulfamethoxazole-Trimethoprim
30
25.8
Tetracycline
72
62.0
0
0.0
24
51.0
Vancomycin
0
0.0
0
0.0
0
0.0
Table 5
Resistance pattern of most common Gram-negative organisms towards antimicrobials
Antimicrobial agents
Gram-negative organisms (% resistant)
P. aeruginosa
Proteus spp.
K. pneumonia
n = 192
(%)
n = 74
(%)
n = 71
(%)
Amikacin
15
8
0
0
0
0
Amoxicillin clavulanic acid
22
11
17
23
13
18
Ampicillin
33
45
56
79
Cefotaxime
0
0
5
7
Ceftazidime
20
10
Cefuroxime
2
1
6
8
6
8
Ciprofloxacin
34
18
12
16
10
14
Gentamicin
16
8
13
18
8
11
Imipenem
17
9
0
0
0
0
Piperacillin
17
9
10
14
27
38
Piperacillin-Tazobactam
34
18
0
0
3
4
Sulphonamides Trimethoprim
17
23
Table 6
Susceptibility pattern of most common anaerobic bacterial isolates towards antimicrobials
Antimicrobial agents
Proportion susceptible (%)
Anaerobic Streptococci
Bacteroides species
Clostridium species
Fusobacterium species
n = 18
(%)
n = 84
(%)
n = 6
(%)
n = 5
(%)
Amoxicillin
Ampicillin/CA
18
100
84
100
6
100
5
100
Erythromycin
18
100
25
30
Cefoxitin
18
100
84
100
6
100
Clindamycin
12
67
27
32
Metronidazole
18
100
84
100
6
100
5
100
Penicillin-G
18
100
3
4
6
100
Piperacillin
18
100
75
89
6
100
Piperacillin/tazobactam
18
100
84
100
6
100
5
100
Tetracycline
Vancomycin

Discussion

DFIs are a burgeoning predicament in Malaysia owing to the high incidence of DM among Malaysians where 1/5th of the population aged more than 30 years old were diagnosed with DM Type 2 reported by Bajuri et al. [16]. Our particular study features significant elements including the etiological agents of DFIs which are predominantly polymicrobial and contain both Gram-positive and Gram-negative bacteria. Anaerobes contribute to the infection by approximately 0.25 anaerobic bacteria per culture-positive specimen, with the majority of the aetiological agents being multi-resistant. When detected in DFI’s, anaerobes are commonly isolated from cultures that concurrently harbour aerobes. Notably, the isolation rate of anaerobes was lower than expected in our study despite its prevalence, especially in comparison with a report by Goldstein et al. [17]. There are many factors that may have contributed to this outcome which include suboptimal sampling or transportation of samples in addition to the use of inappropriate mediums. Previous studies stated that DFI’s predominantly and usually harbour Gram-positive aerobes [18]. On the contrary, most of our patient’s, the major infective organisms were gram-negative bacteria [19].
We discovered that the most common single pathogen isolation in diabetic foot infections was S. Aureus [11, 20, 21]. The prevalence of S. Aureus was 76 and 78% in studies according to Goldstein et al. and Kajetan et al. [2123]. However, we have reported a much lower prevalence when compared with earlier reports. This contrast is to be expected as the majority of our patients had severe forms of DFIs which are commonly polymicrobial when compared with mild DFIs that are usually associated with aerobic Gram-positive cocci, such as S. Aureus. Unfortunately, for the past two decades, MRSA has been a pathogen of concern especially with the evolution of community-acquired MRSA [13]. Our study concluded that the MRSA isolation rate increased to nearly four-folds when compared with previous Malaysian studies [5]. This development is likely due to a lack of strict antibiotic prescription guidelines alongside the lack of adherence to infection control measures in the hospital with a higher prevalence of MRSA in the community. If not rectified, these practices will likely alter empirical antimicrobial therapy.
In addition, approximately 25% of our patients demonstrated Streptococci cultures with a large number being S. agalactiae which is also known as group B Streptococcus [24]. This finding came as no surprise as S. agalactiae is a commonly identified DFI pathogen [17, 18]. Enterococci are considered to be commensals and exhibit low virulence, excluding those who are in an immunocompromised state such as those with DM in which commensals may also become opportunistic pathogens. Despite that, based on previous reports by various investigators, a large number of our patients’ DFIs were caused by other different organisms [17].
Previous antimicrobial use, prolonged hospitalizations, chronic wounds, and surgical interventions which are all distinctive of patients with this type of infection in our hospital are likely contributors to the comparatively large prevalence of P. Aeruginosa in this study. Moreover, a high proportion of E.Coli and Klebsiella spp. isolates were positive for ESBLs and comparison with studies in other regions deduced that the incidence of ESBL-producing Klebsiella spp. and E. coli was higher in our population of patients with DFIs [5]. Hence, routine screening towards ESBL-producing Enterobacteriaceae should be emphasised.
Piperacillin–Tazobactam, Amikacin and Imipenem were the greatest advantageous antimicrobials against aerobic Gram-negative bacteria. As for aerobic Gram-positive cocci and anaerobes, the most effective antimicrobials where Vancomycin and Metronidazole respectively [25]. It is vital to ensure meticulous and thoughtful choices of antimicrobial therapy guided by culture findings in addition to the antimicrobial sensitivity patterns of the specific isolates. Our research has brought us to the conclusion that Ciprofloxacin is not to be recommended for empirical treatment in DFIs as it was particularly inactive against many strains of pathogens identified in the infections. Furthermore, initiation of treatment with broad-spectrum antimicrobials including Carbapenems and Piperacillin-Tazobactam for more-extensive chronic moderate and severe infections appears to be a safe measure. Definitive treatment can subsequently be initiated upon confirmation of offending pathogen via culture and sensitivity testing, susceptibility data and the patient’s response to empirical therapy from a clinical aspect. In order to implement targeted and correct antimicrobial therapy, it is essential to have knowledge and awareness of the common offending pathogens in DFIs.
The management of DFIs often calls for combination therapy with surgical intervention in the form of drainage and debridement or osseous resection especially if osteomyelitis was present [26]. In recent studies, recommendations have included treatment with Hyperbaric Oxygen Therapy (HBOT) as an adjunctive treatment in managing chronic DFIs as they can accelerate wound healing and improve patients’ quality of life [27]. The preference of antibiotic therapy is guided by the sensitivity of the bacterial pathogens encountered. Empirical antimicrobial therapy should utilise versatile antibiotics that have a wide coverage including the coverage of Gram-negative microorganisms, Gram-positive microorganisms and anaerobes if they are particularly suspected in infected foot ulcers. Detailed and meticulous microbiological workup is imperative to the selection of proper antibiotics for DFIs. Numerous drugs have been used to treat non-limb-threatening infections including Aminoglycosides, Ampicillin, Penicillin, Beta-lactamase inhibitors, third-generation Cephalosporins, Quinolones, Piperacillin-Tazobactam and Linezolid [13]. It was also found that Enterococci and anaerobes were not responsive to third-generation Cephalosporins, while Streptococci and anaerobes were said to have been less responsive to Fluoroquinolones [5, 28]. The limitation for this study is that the validated diabetic foot infection tool such as Infectious Diseases Society of America/International Working Group (IDSA/IWGDF) classification was not used as it is not been practiced routinely in our centre. Despite that, there is no difference in the management of our diabetic foot infections in compare to the practice that has been published elsewhere.

Conclusion

The common aetiology of the DFIs in our patients was polymicrobial in nature in which P. Aeruginosa and S. Aureus were identified to be the most common agents and there was a low proportion of anaerobic organisms. Vancomycin, Piperacillin–Tazobactam or Imipenem appear to be suitable agents for empirical therapy according to antimicrobial susceptibility data. Clinicians are also encouraged to obtain adequate specimens after wound debridement for proper culture in addition to requesting for prompt microbiological reporting of all organisms which are obtained from the specimens. Considering the limited suitability of antibiotics, determination of the appropriate antimicrobial treatment should be guided by clinical correlation in addition to the local pattern of bacterial aetiology and its sensitivity. On the grounds that DFI’s are of polymicrobial aetiology, it is unlikely for a single antimicrobial agent to be effective against all the probable organisms isolated from diabetic foot infections. The findings of this study further emphasise the need to select antimicrobial treatment should be guided by proven culture results and antimicrobial sensitivity patterns exhibited by isolates. Choosing empirical antibiotic therapy will be guided by many factors including overall patient condition, glycaemic control, the severity of infection, allergies towards medication, prior antibiotic usage, antibiotic activity, excretion and toxicity. It is imperative to identify causative agents, appropriate antibiotic therapy and management of complications of diabetic foot infections in order to accomplish optimal results.

Acknowledgements

Not applicable.
This study was reviewed and approved by the Ethics Committee of the National Medical Research Register (NMRR) using the following code NMRR-18-1093-41211.
Patients were not required to give informed consent in this study as the analysis used anonymous clinical data that were obtained once patients agreed to treatment with written consent.

Competing interests

The authors declared that they have no competing interests.
Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://​creativecommons.​org/​licenses/​by/​4.​0/​. The Creative Commons Public Domain Dedication waiver (http://​creativecommons.​org/​publicdomain/​zero/​1.​0/​) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Onze productaanbevelingen

BSL Podotherapeut Totaal

Binnen de bundel kunt u gebruik maken van boeken, tijdschriften, e-learnings, web-tv's en uitlegvideo's. BSL Podotherapeut Totaal is overal toegankelijk; via uw PC, tablet of smartphone.

Literatuur
1.
go back to reference Moussa M, Alsaeid M, Abdella N, Refai T, Al-Sheikh N, Gomez J. Prevalence of type 2 diabetes mellitus among Kuwaiti children and adolescents. Med Princ Pract. 2008;17(4):270–5.CrossRef Moussa M, Alsaeid M, Abdella N, Refai T, Al-Sheikh N, Gomez J. Prevalence of type 2 diabetes mellitus among Kuwaiti children and adolescents. Med Princ Pract. 2008;17(4):270–5.CrossRef
2.
go back to reference Zimmet P, Alberti K, Shaw J. Global and societal implications of the diabetes epidemic. Nature. 2001;414(6865):782–7.CrossRef Zimmet P, Alberti K, Shaw J. Global and societal implications of the diabetes epidemic. Nature. 2001;414(6865):782–7.CrossRef
3.
go back to reference Zaini A. Where is Malaysia in the midst of the Asian epidemic of diabetes mellitus? Diabetes Res Clin Pract. 2000;50:S23–8.CrossRef Zaini A. Where is Malaysia in the midst of the Asian epidemic of diabetes mellitus? Diabetes Res Clin Pract. 2000;50:S23–8.CrossRef
4.
go back to reference Mustaffa BE. Diabetes epidemic in Malaysia. Med J Malays. 2004;59(3):295–6. Mustaffa BE. Diabetes epidemic in Malaysia. Med J Malays. 2004;59(3):295–6.
5.
go back to reference Raja NS. Microbiology of diabetic foot infections in a teaching hospital in Malaysia: a retrospective study of 194 cases. J Microbiol Immunol Infect. 2007;40:39–44.PubMed Raja NS. Microbiology of diabetic foot infections in a teaching hospital in Malaysia: a retrospective study of 194 cases. J Microbiol Immunol Infect. 2007;40:39–44.PubMed
6.
go back to reference Ramsey SD, Newton K, Blough D, McCulloch DK, Sandhu N, Reiber GE, Wagner EH. Incidence, outcomes, and cost of foot ulcers in patients with diabetes. Diabetes Care. 1999;22(3):382–7.CrossRef Ramsey SD, Newton K, Blough D, McCulloch DK, Sandhu N, Reiber GE, Wagner EH. Incidence, outcomes, and cost of foot ulcers in patients with diabetes. Diabetes Care. 1999;22(3):382–7.CrossRef
7.
go back to reference Al-Hamead Hefni A, Ibrahim A-MR, Attia KM, Moawad MM, El-ramah AF, Shahin MM, Al-Molla M, Abd A-SL. Bacteriological study of diabetic foot infection in Egypt. Arab Soc Med Res. 2013;8:26–32. Al-Hamead Hefni A, Ibrahim A-MR, Attia KM, Moawad MM, El-ramah AF, Shahin MM, Al-Molla M, Abd A-SL. Bacteriological study of diabetic foot infection in Egypt. Arab Soc Med Res. 2013;8:26–32.
8.
go back to reference Jeffcoate W, Harding K. Diabetic foot ulcers. Lancet. 2003;361(9368):1545–51.CrossRef Jeffcoate W, Harding K. Diabetic foot ulcers. Lancet. 2003;361(9368):1545–51.CrossRef
9.
go back to reference Lipsky B. A report from the international consensus on diagnosing and treating the infected diabetic foot. Diabetes Metab Res Rev. 2004;20(S1):S68–77.CrossRef Lipsky B. A report from the international consensus on diagnosing and treating the infected diabetic foot. Diabetes Metab Res Rev. 2004;20(S1):S68–77.CrossRef
10.
go back to reference Frykberg R. An evidence-based approach to diabetic foot infections. Am J Surg. 2003;186(5):44–54.CrossRef Frykberg R. An evidence-based approach to diabetic foot infections. Am J Surg. 2003;186(5):44–54.CrossRef
11.
go back to reference Lipsky BA, Berendt AR, Deery HG, Embil JM, Joseph WS, Karchmer AW, LeFrock JL, Lew DP, Mader JT, Norden C, Tan JS. Diagnosis and Treatment of Diabetic Foot Infections. Plast Reconstr Surg. 2006;117(SUPPLEMENT):212S–38S.CrossRef Lipsky BA, Berendt AR, Deery HG, Embil JM, Joseph WS, Karchmer AW, LeFrock JL, Lew DP, Mader JT, Norden C, Tan JS. Diagnosis and Treatment of Diabetic Foot Infections. Plast Reconstr Surg. 2006;117(SUPPLEMENT):212S–38S.CrossRef
12.
go back to reference Oyibo SO, Jude EB, Tarawneh I, Nguyen HC, Harkless LB, Boulton AJ. A comparison of two diabetic foot ulcer classification systems: the Wagner and the University of Texas wound classification systems. Diabetes Care. 2001;24(1):84–8.CrossRef Oyibo SO, Jude EB, Tarawneh I, Nguyen HC, Harkless LB, Boulton AJ. A comparison of two diabetic foot ulcer classification systems: the Wagner and the University of Texas wound classification systems. Diabetes Care. 2001;24(1):84–8.CrossRef
13.
go back to reference El-Tahawy AT. Bacteriology of diabetic foot. Saudi Med J. 2000;21(4):344–7.PubMed El-Tahawy AT. Bacteriology of diabetic foot. Saudi Med J. 2000;21(4):344–7.PubMed
14.
go back to reference Wayne PA. Performance standards for antimicrobial disk susceptibility tests. Approved standard, Ninth edition. Document M2-A9. CLSI; 2006. Wayne PA. Performance standards for antimicrobial disk susceptibility tests. Approved standard, Ninth edition. Document M2-A9. CLSI; 2006.
15.
go back to reference Wayne PA, National Committee for Clinical Laboratory Standards. Performance Standards for antimicrobial susceptibility testing: 14th Informational Supplement NCCLS Document M100-S14. 2004. Wayne PA, National Committee for Clinical Laboratory Standards. Performance Standards for antimicrobial susceptibility testing: 14th Informational Supplement NCCLS Document M100-S14. 2004.
17.
go back to reference Citron DM, Goldstein EJC, Merriam CV, Lipsky BA, Abramson MA. Bacteriology of moderate-to-severe diabetic foot infections and in vitro activity of antimicrobial agents. J Clin Microbiol. 2007;45(9):2819–28.CrossRef Citron DM, Goldstein EJC, Merriam CV, Lipsky BA, Abramson MA. Bacteriology of moderate-to-severe diabetic foot infections and in vitro activity of antimicrobial agents. J Clin Microbiol. 2007;45(9):2819–28.CrossRef
18.
go back to reference Mantey I, Hill RL, Foster AV, Wilson S, Wade JJ, Edmonds ME. Infection with foot ulcers with Staphylococcus aureus associated with increase mortality in diabetic patients. Commun Dis Public Health. 2000;3(4):288–90.PubMed Mantey I, Hill RL, Foster AV, Wilson S, Wade JJ, Edmonds ME. Infection with foot ulcers with Staphylococcus aureus associated with increase mortality in diabetic patients. Commun Dis Public Health. 2000;3(4):288–90.PubMed
19.
go back to reference Cauton-Valera R, Lianes LRI, Pena AC. Clinical, microbiological profile and outcome of diabetic patients with foot ulcers admitted at the Quirino memorial medical center: January 2000-may 2001. Philipp J Microbiol Infect Dis. 2001;30(3):101–7. Cauton-Valera R, Lianes LRI, Pena AC. Clinical, microbiological profile and outcome of diabetic patients with foot ulcers admitted at the Quirino memorial medical center: January 2000-may 2001. Philipp J Microbiol Infect Dis. 2001;30(3):101–7.
20.
go back to reference Abdulrazak A, Ibrahim Bitar ZI, Al-Shamali AA, Mobasher LA. Bacteriological study of diabetic foot infections. J Diabetes Complicat. 2005;19(3):138–41.CrossRef Abdulrazak A, Ibrahim Bitar ZI, Al-Shamali AA, Mobasher LA. Bacteriological study of diabetic foot infections. J Diabetes Complicat. 2005;19(3):138–41.CrossRef
21.
go back to reference Goldstein E, Citron D, Nesbit C. Diabetic foot infections: bacteriology and activity of 10 oral antimicrobial agents against bacteria isolated from consecutive cases. Diabetes Care. 1996;19(6):638–41.CrossRef Goldstein E, Citron D, Nesbit C. Diabetic foot infections: bacteriology and activity of 10 oral antimicrobial agents against bacteria isolated from consecutive cases. Diabetes Care. 1996;19(6):638–41.CrossRef
22.
go back to reference Kajetan M, Konkoly TM, Jermendy G. Experience with microbiologic studies of diabetic foot. Orv Hetil. 1995;136(40):2161–4.PubMed Kajetan M, Konkoly TM, Jermendy G. Experience with microbiologic studies of diabetic foot. Orv Hetil. 1995;136(40):2161–4.PubMed
23.
go back to reference Santoso M, Yuliana M, Mujono W. Kusdiantomo. Pattern of diabetic foot at Koja regional general hospital, Jakarta, from 1999 to 2004. Acta Med Indones. 2005;37(4):187–9.PubMed Santoso M, Yuliana M, Mujono W. Kusdiantomo. Pattern of diabetic foot at Koja regional general hospital, Jakarta, from 1999 to 2004. Acta Med Indones. 2005;37(4):187–9.PubMed
24.
go back to reference Altrichter Loan C, Legout L, Assal M, Rohner P, Hoffmeyer P, Bernard L. Severe Streptococcus agalactiae infection of the diabetic foot: a deleterious role of Streptococcus agalactiae? Press Medicale. 2005;34(7):491–4.CrossRef Altrichter Loan C, Legout L, Assal M, Rohner P, Hoffmeyer P, Bernard L. Severe Streptococcus agalactiae infection of the diabetic foot: a deleterious role of Streptococcus agalactiae? Press Medicale. 2005;34(7):491–4.CrossRef
25.
go back to reference Ng LSY, Lee LK, Yeow SCS, Thean YT. Anaerobic culture of diabetic foot infections: organisms and antimicrobial susceptibilities. Ann Acad Med Singap. 2008;37(11):936–9.PubMed Ng LSY, Lee LK, Yeow SCS, Thean YT. Anaerobic culture of diabetic foot infections: organisms and antimicrobial susceptibilities. Ann Acad Med Singap. 2008;37(11):936–9.PubMed
26.
go back to reference Bajuri MY, Abdul Razak KA. Chronic osteomyelitis of the femur with segmental bone defect: concepts and treatment. J Krishna Inst Med Sci Univ. 2017;6(2):127–30. Bajuri MY, Abdul Razak KA. Chronic osteomyelitis of the femur with segmental bone defect: concepts and treatment. J Krishna Inst Med Sci Univ. 2017;6(2):127–30.
27.
go back to reference Bajuri MY, Mohd RH. The physiological, biochemical and quality of life changes in chronic diabetic foot ulcer after hyperbaric oxygen therapy. Med Health. 2017;12(2):210–9.CrossRef Bajuri MY, Mohd RH. The physiological, biochemical and quality of life changes in chronic diabetic foot ulcer after hyperbaric oxygen therapy. Med Health. 2017;12(2):210–9.CrossRef
28.
go back to reference Ge Y, MacDonald D, Hait H, Lipsky B, Zasloff M, Holroyd K. Microbiological profile of infected diabetic foot ulcers. Diabet Med. 2002;19(12):1032–4.CrossRef Ge Y, MacDonald D, Hait H, Lipsky B, Zasloff M, Holroyd K. Microbiological profile of infected diabetic foot ulcers. Diabet Med. 2002;19(12):1032–4.CrossRef
Metagegevens
Titel
Clinical and bacteriological profile of diabetic foot infections in a tertiary care
Auteurs
Teik Chiang Goh
Mohd Yazid Bajuri
Sivapathasundaram C. Nadarajah
Abdul Halim Abdul Rashid
Suhaila Baharuddin
Kamarul Syariza Zamri
Publicatiedatum
01-12-2020
Uitgeverij
BioMed Central
Gepubliceerd in
Journal of Foot and Ankle Research / Uitgave 1/2020
Elektronisch ISSN: 1757-1146
DOI
https://doi.org/10.1186/s13047-020-00406-y

Andere artikelen Uitgave 1/2020

Journal of Foot and Ankle Research 1/2020 Naar de uitgave