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

Clinical data	Group 1 (n = 115)		Group 2 (n = 22)
Clinical data	n	%	n	%
Type 1 diabetes	13	11.3	2	9.1
Type 2 diabetes	91	79.1	20	90.9
Other specific types of diabetes	9	7.8	0	-
No data on the type of diabetes	2	1.7	0	-
Male	87	75.7	16	72.7
Female	28	24.3	6	27.3
Neuropathic foot ulcers	52	45.2	14	63.6
Neuro-ischemic foot ulcers	50	43.5	7	31.8
Ischemic foot ulcers	11	9.6	1	4.5
Indeterminate type	2	1.7	0	-
Obesity	46	40.0	14	63.6
Overweight	16	13.9	4	18.9
Normal weight	25	21.7	3	13.6
Lack of body weight data	28	24.4	1	4.5
Age in years ± SD	59.7±10.02		58.5±9.68
Duration of diabetes in years ± SD	17.03±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 growth	16 (11.7%)	1 (1.6%)
one microorganism	49 (35.8%)	21 (33.3%)
two microorganisms	33 (24.0%)	17 (27.0%)
three microorganisms	13 (9.5%)	13 (20.6%)
more than three microorganisms	26 (19.0%)	11 (17.5%)

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

Hba1c %	<6.0	6.0–6.9	7.0–7.9	8.0–8.9	9.0–9.9	10.0–10.9	11.0–11.9	>12
Group 1	7.8%	34.3%	23.5%	20.6%	7.8%	2.0%	2.9%	1.0%
Group 2	2.1%	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

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

Enterobacterales:	145/37.56%
1. Enterobacteriaceae	41/10.62%
E. coli * including 1 strain ESBL(+)	15/3,89%
E. cloacae * including 2 strains ESBL(+)	9
Enterobacter spp.	2
E. amnigenus	1
K. oxytoca	5
K. pneumoniae * including 2 strains ESBL(+)	3
C. freundii	5
C. braakii	1
2. Yersiniaceae	49/12.69%
S. marcescens	48/12,43%
Serratia spp.	1
3. Hafniaceae	1/0.26%
H. alvei	1
4. Morganellaceae	54/13.99%
P. mirabilis	27
P. vulgaris	9
P. penneri	1
M. morganii	14
P. stuartii	2
P. rettgeri	1
Pseudomonas aeruginosa	27/6.99%
* 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 antibiotics	7
A. haemolyticus	1
A. pittii	1
Other Gram-negative rods: A. hydrophila, A. faecalis, P. multocida, B. cepacia	6/1.55%

Fungi: in total 3/0.78%

Candida spp.	3/0.78%
C. albicans	2
C. parapsilosis	1

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

Staphyloccous aureus	46/11.92 %
* including 14 (3.63%) MRSA strains Coagulase negative staphylococci
S. epidermidis	11/2.85 %
S. simulans	7
S. haemolyticus	2
S. cohnii	1
Streptococcus spp.	1
S. agalactiae	34/8.81 %
Streptococcus spp.	9
β-haemolytic streptococci group C,	7
G and F	5
S. dysgalactiae
S. oralis	4
S. intermedius	4
S. mitis, S. anginosus, S. sanguinis	2
Enterococcus spp.	3
E. faecalis	12/3.11%
E. faecium	11/2,85%
Other Gram-positive bacteria:	1
Corynebacterium spp., Leuconostoc spp., D. hominis, H. kunzi, M. luteus	10/2.59%

Anaerobes: in total 83/21.5%

Peptostreptococcus spp.	21/5.44 %
F. magna	11/2.85 %
B. fragilis	5
B. thetaiotaomicron	4
B. ovatus	1
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

Microorganism	Hba1c mean value	HBA1c ± SD	HbA1c <8	HbA1c 8-12,3	Lack of HbA1c measurements
Pseudomonas aeruginosa	7.2	0.9	71.4%	14.3%	14.3%
Peptostreptococcus spp.	7.4	1.1	66.7%	23.8%	9.5%
Serratia marcescens	7.5	1.1	62.0%	32.0%	6.0%
Proteus mirabilis	7.7	1.0	42.9%	39.3%	17.8%
Staphylococcus aureus MSSA*	7.9	1.4	59.1%	38.6%	2.3%
Escherichia coli	8.1	1.5	43.75%	50.0%	6.25%
Morganella morganii	8.8	1.1	18.75%	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

Bacteria	N	Mean ± SD	Median	Min	Max	CV^* [%]	SEM^**
Serratia marcescens	47	7.5 ± 1.1	7.4	5.2	9.7	14.9	0.2
MSSA	43	7.9 ± 1.4	7.7	5.7	12.3	18.1	0.2
Pseudomonas aeruginosa	24	7.2 ± 0.9	7.3	6.1	9.0	12.4	0.2
Proteus mirabilis	23	7.6 ± 1	7.4	5.9	9.1	13.7	0.2
Peptostreptococcus spp.	19	7.4 ± 1.1	7.4	6.0	9.6	14.9	0.3
Escherichia coli	15	8.1 ± 1.5	8.2	5.9	11.1	18.5	0.4
Morganella morganii	12	8.8 ± 1.1	8.7	7.2	11.1	12.5	0.3

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

Publication	I	II	III	IV	V	VI	VII	VIII	IX	X	XI
Year of publication	2006	2007	2009	2011	2011	2014	2014	2015	2016	2018	2020
Number of patients	80	433	379	434	440	196	102	41	447	261	137
Microorganism in
Staphylococcus aureus MSSA^*	13.7	14.3	17.3	13.8	3.0	21.0	13.6	30.0	9.6	26.9	8.3
Staphylococcus aureus MRSA^**	13.7	4.4	11.3	N/A	8.0	N/A	1.0	N/A	1.8		3.6
Streptococus spp.	N/A	15.5	12.6	3.0	4.0	4.7	3.0	9.0	7.2	1.7	8.8
Enterococcus spp.	11.5	13.6	7.7	9.5	6.0	3.4	16.0	N/A	4.4	12.7	3.1
coagulase-negative Staphylococci	6.6	15.2	14.9	5.0	0.5	N/A	11.5	N/A	1.3	N/A	2.8
Escherichia coli	12.0	1.7	N/A	16.1	6.0	28.6	7.0	4.5	15.0	12	3.9
Proteus mirabilis	12.6	2.1	N/A	8.8	6.0	4.2	7.6	11.0	9.6	3.1	7.0
Pseudomonas aeruginosa	9.8	3.5	6.9	16.9	17.0	N/A	7.5	4.5	12.4	20.9	7.0
Acinetobacter spp.	9.3	1.1	N/A	3.7	N/A	4.2	2.0	N/A	2.8	1	2.3
Klebsiella spp.	6.6	2.2	N/A	6.7	5.0	14.3	3.5	N/A	3.4	9.5	2.1
Serratia marcescens	N/A	1.2	N/A	N/A	2.0	N/A	2.0	N/A	1.6	0.3	12.4
Morganella morganii	N/A	N/A	N/A	N/A	3.0	N/A	1.5	N/A	4.9	N/A	3.6
Peptostreptococcus spp.	1.6	N/A	N/A	N/A	N/A	N/A	1.5	N/A	N/A	N/A	5.4
Bacteroides fragilis	1.6	4.1	N/A	N/A	N/A	N/A	1.0	N/A	N/A	N/A	1.3

eISSN:: 1732-2693
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Analysis of the microbiota in the diabetic foot ulcers: Is research standardization required?

Article Category: Original Article

Published Online: May 25, 2021

Page range: 362 - 370

Received: May 12, 2020

Accepted: Feb 02, 2021

DOI: https://doi.org/10.5604/01.3001.0014.8987

Keywordsdiabetic foot ulcer, microbiological culture, HbA1c values, wound infection

© 2021 Marta Margas et al., published by Sciendo

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Characteristics of patients in group 1 and 2

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

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

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

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

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

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

Keywords
diabetic foot ulcer, microbiological culture, HbA1c values, wound infection