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Phenotypic and genetic properties of susceptible and multidrug-resistant Pseudomonas aeruginosa isolates in Southern Serbia

Marko Milojković
Marko Milojković
, 
Željka Nenadović
Željka Nenadović
, 
Slaviša Stanković
Slaviša Stanković
, 
Dragana D. Božić
Dragana D. Božić
, 
Nataša Stanković Nedeljković
Nataša Stanković Nedeljković
, 
Ivana Ćirković
Ivana Ćirković
, 
Marija Petrović
Marija Petrović
 und 
Ivica Dimkić
Ivica Dimkić
   | 06. Okt. 2020
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Article Category: Original article
Online veröffentlicht: 06. Okt. 2020
Seitenbereich: 231 - 250
Eingereicht: 01. Apr. 2020
Akzeptiert: 01. Aug. 2020
DOI: https://doi.org/10.2478/aiht-2020-71-3418
Schlüsselwörter
© 2020 Marko Milojković et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Figure 1

Susceptibility of clinical isolates of Pseudomonas spp. on different antibiotic classes. The isolates were classified as resistant (R), intermediate (I), or susceptible (S)
Susceptibility of clinical isolates of Pseudomonas spp. on different antibiotic classes. The isolates were classified as resistant (R), intermediate (I), or susceptible (S)

Figure 2

Dendrogram obtained by UPGMA analysis of the selected Pseudomonas isolates using 208 (top) and 272 (bottom) primers, based on RADP profile (right). Genetic distances were presented with numbers placed on the branches. Rectangles are representing the isolate grouping according to obtained RAPD patterns
Dendrogram obtained by UPGMA analysis of the selected Pseudomonas isolates using 208 (top) and 272 (bottom) primers, based on RADP profile (right). Genetic distances were presented with numbers placed on the branches. Rectangles are representing the isolate grouping according to obtained RAPD patterns

Figure 3

Dendrogram obtained by UPGMA analysis of the selected Pseudomonas isolates using BOX (top) and ERIC (bottom) primers, based on rep-PCR profile (right). Genetic distances were presented with numbers placed on the branches. Rectangles are representing the isolate grouping according to obtained rep-PCR patterns
Dendrogram obtained by UPGMA analysis of the selected Pseudomonas isolates using BOX (top) and ERIC (bottom) primers, based on rep-PCR profile (right). Genetic distances were presented with numbers placed on the branches. Rectangles are representing the isolate grouping according to obtained rep-PCR patterns

Figure 4

Phylogenetic relationships of Pseudomonas aeruginosa clinical isolates from all 12 RAPD272 clusters based on the sequence of 16S rRNA. Phylogenetic tree was constructed by the neighbour-joining method and the distances were calculated with the Kimura two-parameter model. Bootstrap values are given for each node, with 1000 replicates. Stenotrophomonas maltophilia was used as an outgroup. The horizontal bar indicates a genetic distance of 0.02
Phylogenetic relationships of Pseudomonas aeruginosa clinical isolates from all 12 RAPD272 clusters based on the sequence of 16S rRNA. Phylogenetic tree was constructed by the neighbour-joining method and the distances were calculated with the Kimura two-parameter model. Bootstrap values are given for each node, with 1000 replicates. Stenotrophomonas maltophilia was used as an outgroup. The horizontal bar indicates a genetic distance of 0.02

Multidrug resistant Pseudomonas spp. isolates and their pigmentation, serotype, and biofilm formation potential

Minimum inhibitory concentration (MIC, expressed in μg/mL) of inpatient and outpatient Pseudomonas spp. isolates and their potential to produce beta-lactamases

Inpatients Outpatients
Isolate coded name Specimen Mer Ceft Cef Enzyme produced Isolate name coded Specimen Mer Ceft Cef Enzyme produced
5660 Throat <1 4 8 - 2609 Ear <1 <2 <2 -
5661 Throat <1 <2 <2 - 4278 Ear <1 <2 <2 -
1183 Urine >16 16 4 - 5518 Ear >16 16 32 MBL
2638 Urine >16 >32 >32 CRP 7546 Ear <1 <2 <2 -
2844 Urine <1 <2 16 - 294 Sputum <1 <2 <2 -
3853 Urine 4 16 4 - 2124 Sputum 2 >32 >32 -
611 Wound <1 <2 <2 - 2941 Sputum <1 <2 <2 -
821 Wound >16 4 2 - 2966 Sputum <1 2 4 -
971 Wound <1 32 16 - 3496 Sputum <1 >32 >32 -
1087 Wound >16 >32 >32 CRP 3919 Sputum <1 4 4 -
1416 Wound <1 4 4 - 8142 Sputum <1 4 4 -
2064 Wound <1 16 <2 - 9921 Sputum 2 16 16 -
2073 Wound >16 >32 >32 CRP 11838 Sputum <1 <2 <2 -
2581 Wound <1 16 8 MBL 1863 Throat <1 <2 <2 -
2645 Wound >16 >32 >32 CRP 2005 Throat <1 2 2 -
2900 Wound >16 >32 >32 CRP 2047 Throat <1 <2 <2 -
3122 Wound <1 8 8 - 3238 Throat <1 4 4 -
3322 Wound 16 2 2 MBL 3477 Throat <1 2 2 -
3451 Wound <1 16 8 - 3540 Throat <1 4 2 -
3563 Wound <1 4 4 - 3864 Throat <1 2 2 -
3595 Wound <1 4 4 - 4087 Throat <1 4 4 -
3658 Wound <1 4 2 - 4646 Throat <1 2 2 -
3714 Wound >16 32 >32 MBL 9642 Throat <1 <2 <2 -
3883 Wound 2 <2 <2 - 10412 Throat <1 4 4 -
4071 Wound <1 4 4 - 2383 Tongue <1 4 4 -
4082 Wound <1 4 4 - 2967 Tongue <1 16 32 -
4211 Wound <1 16 8 - 1408 Urine <1 <2 <2 -
4212 Wound <1 4 4 - 1790 Urine <1 4 4 -
4312 Wound <1 16 2 - 2285 Urine <1 2 2 -
4314 Wound <1 2 2 - 2588 Urine 16 2 4 -
4354 Wound <1 2 2 - 2597 Urine <1 4 16 ESBL
4473 Wound <1 8 8 - 2711 Urine <1 4 16 MBL
4541 Wound <1 <2 <2 - 2875 Urine <1 2 2 -
5348 Wound <1 2 4 - 3199 Urine <1 4 4 -
5774 Wound 4 4 16 - 3214 Urine 1 >32 16 -
5797 Wound 2 >32 2 - 3777 Urine >16 4 16 CRP
6412 Wound <1 2 2 - 4188 Urine >16 4 32 CRP
6982 Wound <1 <2 <2 - 4362 Urine <1 16 16 -
7543 Wound 1 16 16 ESBL 5586 Urine <1 <2 <2 -
7698 Wound <1 4 4 - 8599 Urine >16 32 8 -
7881 Wound <1 2 2 - 10019 Urine <1 8 16 -
8283 Wound <1 <2 <2 - 10600 Urine <1 16 4 -
8702 Wound <1 <2 <2 - 2671 Vag. swab <1 2 2 -
8913 Wound <1 <2 <2 - 2689 Vag. swab <1 16 8 -
10195 Wound <1 >32 >32 -
10336 Wound <1 <2 <2 -
10708 Wound <1 4 2 -
10800 Wound <1 32 8 CRP
11947 Wound <1 2 2 -
19677 Wound <1 4 4 -

Antibiotic susceptibility of inpatient and outpatient Pseudomonas spp. isolates

Inpatients
Isolate coded name Specimen Aminoglycosides Fluoroquinolones Polyp Monob Penicillin comb. Carbapenems Cephalosporins
Amik Gent Net Tobr Oflox Cipr Levofl Col Aztr Pip/taz Dor Imp Mer Ceft Cef
5660 Throat S S S S S S S S S S S S S S S
5661 Throat S S S S S S S S S S S S S S S
1183 Urine S R R R R R R S S S S S R R S
2638 Urine R R R R R R R S S R R R R R R
2844 Urine S R S R R R R S S S S S S S R
3853 Urine S R R R R R R S S S S S S R S
611 Wound S S S S S S S S S S S S S S S
821 Wound S S S S S S S S S S S S R S S
971 Wound S S S S S S S S S S S S S R R
1087 Wound R R R R R R R S S R R R R R R
1416 Wound S S S S R S S S S S S S S S S
2064 Wound S S R S S S S S S S S S S R S
2073 Wound R R R R R R R S S S R R R R R
2581 Wound R R R R R R R S S R S S S R S
2645 Wound R R R R R R R S S R R R R R R
2900 Wound R R R R R R R S S S R R R R R
3122 Wound S S R S R S S S S S S S S S S
3322 Wound R R R R R R R S S R S S R S S
3451 Wound S R R R R R R S S R S S S R S
3563 Wound R R R R R R R S S S S S S S S
3595 Wound S S S S S S S S S S S S S S S
3658 Wound S R R R R R R S S S R S S S S
3714 Wound S S S R S S S S R S S R R R R
3883 Wound S S S S S S S S S S S S S S S
4071 Wound S S S S S S S S S S S S S S S
4082 Wound S S S S S S S S S S S S S S S
4211 Wound S S S S S S S S S S S S S R S
4212 Wound S S S S S S S S S S S S S S S
4312 Wound R R R S R R S S S S S S S R S
4314 Wound S S S S S S S S S S S S S S S
4354 Wound S S S S S S S S S S S S S S S
4473 Wound S S S S S S S S S S S S S S S
4541 Wound S S S S S S S S S S S S S S S
5348 Wound R R R R R R R S S R S S S S S
5774 Wound R R R R R R R S S S S S I S R
5797 Wound R R R R R R R S S S S S S R S
6412 Wound S S S S S S S S S S S S S S S
6982 Wound S S S S S S S S S S S S S S S
7543 Wound R R R R R R R S S R S S S R R
7698 Wound R R I R S I S S S S S S S S S
7881 Wound S S R S S S S S S S S S S S S
8283 Wound I I R R R R R S S S S S S S S
8702 Wound S S S S S S S S S S S S S S S
8913 Wound R R R R R R R S S S S S S S S
10195 Wound S S S S R I I S S S S S S R R
10336 Wound S S S S S S S S S S S S S S S
10708 Wound R I I S S S S S S S S S S S S
10800 Wound S I S S S S S S S S R R S R S
11947 Wound S S S S S S S S S S S S S S S
19677 Wound S S S S S S S S S S S S S S S
Outpatients
Isolate coded name Specimen Aminoglycosides Fluoroquinolones Polyp Monob Penicillin comb. Carbapenems Cephalosporins
Amik Gent Net Tobr Oflox Cipr Levofl Col Aztr Pip/taz Dor Imip Mer Ceft Cef
2609 Ear S S S S S S S S S R S S S S S
4278 Ear S I S S S S S S S S S S S S S
5518 Ear S S S S S S S S S S S S R R R
7546 Ear S S S S S S S S S S S S S S S
294 Sputum S R S I S S S S S S S S S S S
2124 Sputum S S S R R R R S S R S S S R R
2941 Sputum S S S S S S S S S S S S S S S
2966 Sputum S S S S S S S S S S S S S S S
3496 Sputum S S S S S S S S S S S S S R R
3919 Sputum S S S S S S S S S S S S S S S
8142 Sputum S R S S S S S S S S S S S S S
9921 Sputum R R R R R R R S S S S S S R R
11838 Sputum S R S S R S S S S S S S S S S
1863 Throat S S S S S S S S S S S S S S S
2005 Throat S S S S S S S S S S S S S S S
2047 Throat S S S S S S S S S S S S S S S
3238 Throat S S S S S S S S S S S S S S S
3477 Throat S S S S S S S S S S S S S S S
3540 Throat S S S S S S S S S S S S S S S
3864 Throat S I S S S S S S S S S S S S S
4087 Throat S S S S S S S S S S S S S S S
4646 Throat S S S S S S S S S S S S S S S
9642 Throat S S S S S S S S S S S S S S S
10412 Throat S S S S S S S S S S S S S S S
2383 Tongue S R S S S S S S S R S S S S S
2967 Tongue I R R R S S S S S R S S S R R
1408 Urine R R S R R R R S S S S S S S S
1790 Urine I R S S S S S S S S S S S S S
2285 Urine S S S S S S S S S S S S S S S
2588 Urine R R R R R R I S S S S S R S S
2597 Urine S R R R R R R S R S S S S S R
2711 Urine R I R R S S R S S S S R S S R
2875 Urine R R S R R R R S S S S S S S S
3199 Urine S R R R R R R S S S S S S S S
3214 Urine S R R R R R R S S R S S S R R
3777 Urine S R R R R R R S S S R S R S R
4188 Urine I R R R R R R S S S R S R S R
4362 Urine S S S S S S S S S S S S S R R
5586 Urine S S S S S S S S S S S S S S S
8599 Urine S R R R R R R S S S S S R R S
10019 Urine R R R R R R R S S I S S S S R
10600 Urine S S S S S S S S S R S S S R S
2671 Vag. Swab S S S S S S S S S S S S S S S
2689 Vag. Swab S S S S S S S S S S S S S R S

Selected isolates for further molecular genetic analysis

Group I Group II Group III Group IV Group V
Resistant up to 4 antibiotic classes or more Resistant up to 3 antibiotic classes Resistant up to 2 antibiotic classes Resistant up to 1 antibiotic class Susceptible to all tested antibiotic classes
Isolate coded name Group cipher Isolate coded name Group cipher Isolate coded name Group cipher Isolate coded name Group cipher Isolate coded name Group cipher
2711 1-1 5797 2-1 8283 3-1 2609 4-1 3864 5-1
7543 1-2 4312 2-2 5518 3-2 821 4-2 2047 5-2
2597 1-3 5348 2-3 10195 3-3 4362 4-3 6412 5-3
3714 1-4 10019 2-4 3563 3-4 1790 4-4 3238 5-4
2645 1-5 3658 2-5 3122 3-5 7881 4-5 11947 5-5
3777 1-6 2967 2-6 10800 3-6 4211 4-6
2900 1-7 2844 2-7 2064 3-7 3496 4-7
3451 1-8 3853 2-8 11838 3-8 8142 4-8
2124 1-9 2588 2-9 1408 3-9 971 4-9
4188 1-10 9921 2-10 2383 3-10 2689 4-10

Serological identification of polyvalent and monovalent serotypes, pigmentation, and biofilm formation of Pseudomonas spp. clinical isolate of different origin

Polyvalent and monovalent serotypes Pigments type Biofilm formation
Isolate origin PMA PME PMC PMF NT Pyov+ Pyoc Pyov Pyoc Cat. 0(-) Cat. 1(+) Cat. 2(++) Cat. 3(+++)
P1 P6 P5 P9 P10 P11
Throat 4 4 - - 1 1 3 9 3 1 2 6 5 -
Tongue - 1 - - 1 - - 1 1 - 1 - 1 -
Wound 7 7 3 6 - 8 13 30 12 2 12 17 14 1
Cer-vagmal canal - - - - - - 2 1 1 - 1 - 1 -
Ear - 2 - - - 1 1 2 1 1 - - 4 -
Sputum 1 4 - 1 - 1 2 7 1 1 2 4 1 2
Urine culture 4 3 - 2 - 4 7 16 2 2 3 12 3 2
Σtotal isloates 16 21 3 9 2 15 28 66 21 7 21 39 29 5
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