Have a personal or library account? Click to login

Analysis of the microbiota in the diabetic foot ulcers: Is research standardization required?

Open Access
|May 2021

Figures & Tables

Characteristics of patients in group 1 and 2

Clinical dataGroup 1 (n = 115)Group 2 (n = 22)
n%n%
Type 1 diabetes1311.329.1
Type 2 diabetes9179.12090.9
Other specific types of diabetes97.80-
No data on the type of diabetes21.70-
Male8775.71672.7
Female2824.3627.3
Neuropathic foot ulcers5245.21463.6
Neuro-ischemic foot ulcers5043.5731.8
Ischemic foot ulcers119.614.5
Indeterminate type21.70-
Obesity4640.01463.6
Overweight1613.9418.9
Normal weight2521.7313.6
Lack of body weight data2824.414.5
Age in years ± SD59.7±10.02 58.5±9.68
Duration of diabetes in years ± SD17.03±10.36 16.9±12.09

Results of microbiological cultures in terms of the number of microorganisms isolated in the culture in group 1 and 2

Results of cultures (n = 200)Group 1 (n = 137)Group 2 (n = 63)
no growth16 (11.7%)1 (1.6%)
one microorganism49 (35.8%)21 (33.3%)
two microorganisms33 (24.0%)17 (27.0%)
three microorganisms13 (9.5%)13 (20.6%)
more than three microorganisms26 (19.0%)11 (17.5%)

Percentage of HbA1c values of patients in the group 1 and 2

Hba1c %<6.06.0–6.97.0–7.98.0–8.99.0–9.910.0–10.911.0–11.9>12
Group 17.8%34.3%23.5%20.6%7.8%2.0%2.9%1.0%
Group 22.1%25.0%29.2%20.8%20.8%0.0%0.0%2.1%

Quantitative and percentage distribution of microbial species isolated from wounds in patients with DFU in both study groups

MicroorganismNumber/percent
Aerobic and facultatively anaerobic Gram-negative rods: in total 187/48,44%

Enterobacterales:145/37.56%
1. Enterobacteriaceae41/10.62%
E. coli * including 1 strain ESBL(+)15/3,89%
E. cloacae * including 2 strains ESBL(+)9
Enterobacter spp.2
E. amnigenus1
K. oxytoca5
K. pneumoniae * including 2 strains ESBL(+)3
C. freundii5
C. braakii1
2. Yersiniaceae49/12.69%
S. marcescens48/12,43%
Serratia spp.1
3. Hafniaceae1/0.26%
H. alvei1
4. Morganellaceae54/13.99%
P. mirabilis27
P. vulgaris9
P. penneri1
M. morganii14
P. stuartii2
P. rettgeri1
Pseudomonas aeruginosa27/6.99%
* including 3 strains resistant to carbapenems, 3 strains resistant to ≥2 antibiotics
Acinetobacter spp.9/2.33 %
A. baumannii * including 2 strains resistant to carbapenems,3 strains resistant to ≥2 antibiotics7
A. haemolyticus1
A. pittii1
Other Gram-negative rods: A. hydrophila, A. faecalis, P. multocida, B. cepacia6/1.55%

Fungi: in total 3/0.78%

Candida spp.3/0.78%
C. albicans2
C. parapsilosis1

Facultatively anaerobic Gram-positive bacteria: in total 113/29,27%

Staphyloccous aureus46/11.92 %
* including 14 (3.63%) MRSA strains Coagulase negative staphylococci
S. epidermidis11/2.85 %
S. simulans7
S. haemolyticus2
S. cohnii1
Streptococcus spp.1
S. agalactiae34/8.81 %
Streptococcus spp.9
β-haemolytic streptococci group C,7
G and F5
S. dysgalactiae
S. oralis4
S. intermedius4
S. mitis, S. anginosus, S. sanguinis2
Enterococcus spp.3
E. faecalis12/3.11%
E. faecium11/2,85%
Other Gram-positive bacteria:1
Corynebacterium spp., Leuconostoc spp., D. hominis, H. kunzi, M. luteus10/2.59%

Anaerobes: in total 83/21.5%

Peptostreptococcus spp.21/5.44 %
F. magna11/2.85 %
B. fragilis5
B. thetaiotaomicron4
B. ovatus1
Prevotella spp.7
Peptoniphilus spp.7
Anaerococcus spp.7
Peptococcus spp.6
Fusobacterium spp.5
Veillonella spp.4
Actinomyces spp.2
Porphyromonas spp.1

Percentage distribution of HbA1c values in patients with selected microorganisms isolated in the culture

MicroorganismHba1c mean valueHBA1c ± SDHbA1c <8HbA1c 8-12,3Lack of HbA1c measurements
Pseudomonas aeruginosa7.20.971.4%14.3%14.3%
Peptostreptococcus spp.7.41.166.7%23.8%9.5%
Serratia marcescens7.51.162.0%32.0%6.0%
Proteus mirabilis7.71.042.9%39.3%17.8%
Staphylococcus aureus MSSA*7.91.459.1%38.6%2.3%
Escherichia coli8.11.543.75%50.0%6.25%
Morganella morganii8.81.118.75%56.25%25.0%

Median and interquartile range and minimum and maximum values of HBA1c concentration in groups of patients infected with different strains of bacteria

BacteriaNMean ± SDMedianMinMaxCV* [%]SEM**
Serratia marcescens477.5 ± 1.17.45.29.714.90.2
MSSA437.9 ± 1.47.75.712.318.10.2
Pseudomonas aeruginosa247.2 ± 0.97.36.19.012.40.2
Proteus mirabilis237.6 ± 17.45.99.113.70.2
Peptostreptococcus spp.197.4 ± 1.17.46.09.614.90.3
Escherichia coli158.1 ± 1.58.25.911.118.50.4
Morganella morganii128.8 ± 1.18.77.211.112.50.3

Microorganisms isolated from clinical samples obtained from patients with DFU in various geographical zones

PublicationIIIIIIIVVVIVIIVIIIIXXXI
Year of publication20062007200920112011201420142015201620182020
Number of patients8043337943444019610241447261137
Microorganism in
Staphylococcus aureus MSSA*13.714.317.313.83.021.013.630.09.626.98.3
Staphylococcus aureus MRSA**4.411.3N/A8.0N/A1.0N/A1.8 3.6
Streptococus spp.N/A15.512.63.04.04.73.09.07.21.78.8
Enterococcus spp.11.513.67.79.56.03.416.0N/A4.412.73.1
coagulase-negative Staphylococci6.615.214.95.00.5N/A11.5N/A1.3N/A2.8
Escherichia coli12.01.7N/A16.16.028.67.04.515.0123.9
Proteus mirabilis12.62.1N/A8.86.04.27.611.09.63.17.0
Pseudomonas aeruginosa9.83.56.916.917.0N/A7.54.512.420.97.0
Acinetobacter spp.9.31.1N/A3.7N/A4.22.0N/A2.812.3
Klebsiella spp.6.62.2N/A6.75.014.33.5N/A3.49.52.1
Serratia marcescensN/A1.2N/AN/A2.0N/A2.0N/A1.60.312.4
Morganella morganiiN/AN/AN/AN/A3.0N/A1.5N/A4.9N/A3.6
Peptostreptococcus spp.1.6N/AN/AN/AN/AN/A1.5N/AN/AN/A5.4
Bacteroides fragilis1.64.1N/AN/AN/AN/A1.0N/AN/AN/A1.3
Language: English
Page range: 362 - 370
Submitted on: May 12, 2020
Accepted on: Feb 2, 2021
Published on: May 25, 2021
Published by: Hirszfeld Institute of Immunology and Experimental Therapy
In partnership with: Paradigm Publishing Services
Publication frequency: 1 issue per year

© 2021 Marta Margas, Marta Wróblewska, Halina Marchel, Beata Mrozikiewicz-Rakowska, Piotr Ładyżyński, Ewa Wojciechowska, Leszek Czupryniak, Janusz Krzymień, published by Hirszfeld Institute of Immunology and Experimental Therapy
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.