Prevalence of carbapenemase genes among multidrug-resistant Pseudomonas aeruginosa isolates from tertiary care centers in Southern Thailand

Phanvasri Saengsuwan; Narongdet Kositpantawong; Soontara Kawila; Wichien Patugkaro; Chonticha Romyasamit

doi:10.15537/smj.2022.43.9.20220219

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Figure 1
- Dendrogram of Pseudomonas aeruginosa isolated from CR-MDR-PA in tertiary care hospitals of Songkhla Province. The PFGE profiles were analyzed using the BioNumerics software, the similarity of band patterns was computed using Pearson’s correlation coefficient, and a dendrogram was generated using an unweighted pair group of the arithmetic mean approach. The isolates were clustered into groups with >70% similarity. The scale represents the percentage of similarity. CR-MDR-PA: carbapenem-resistant multidrug-resistant Pseudomonas aeruginosa, PFGE: pulsed field gel electrophoresis
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Appendix 1
- The occurrence of 289 Pseudomonas aeruginosa (P. aeruginosa) isolated from various specimens in tertiary care hospitals of Songkhla Province between August 2015 and March 2017.
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Appendix 2
- Multiplex PCR-based genotypic characterization of Pseudomonas aeruginosa (P. aeruginosa) isolates recovered from clinicsl isolates. Lane M: 100 bp molecular size marker, Lane 1-5: clinical P. aeruginosa isolates showing band at 232 bp denoting bla_IMP, bla_VIM, bla_OXA48, bla_NDM, bla_DIM, and bla_SIM gene band at 390, 438, 621, 699, and 570 bp, Lane 6-8: multiplex PCR were control strains

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Table 1

- List of primers used for amplifying carbapenemase genes.

Primer	Sequence (5′→3′)	Genes	Product sizes (bp)
IMP-F	GGAATAGAGTGGCTTAAYTCTC	bla_IMP	232
IMP-R	GGTTTAAYAAAACAACCACC
SPM-F	AAAATCTGGGTACGCAAACG	bla_SPM	271
SPM-R	ACATTATCCGCTGGAACAGG
AIM-F	CTGAAGGTGTACGGAAACAC	bla_AIM	322
AIM-R	GTTCGGCCACCTCGAATTG
VIM-F	GATGGTGTTTGGTCGCATA	bla_VIM	390
VIM-R	CGAATGCGCAGCACCAG
OXA-F	GCGTGGTTAAGGATGAACAC	bla_OXA-48	438
OXA-R	CATCAAGTTCAACCCAACCG
GIM-F	TCGACACACCTTGGTCTGAA	bla_GIM	477
GIM-R	AACTTCCAACTTTGCCATGC
BIC-F	TATGCAGCTCCTTTAAGGGC	bla_BIC	537
BIC-R	TCAATTGGCGGTGCCGTACAC
SIM-F	TACAAGGGATTCGGCATCG	bla_SIM	570
SIM-R	TAATGGCCTGTTCCCATGTG
NDM-F	GGTTTGGCGATCTGGTTTTC	bla_NDM	621
NDM-R	CGGAATGGCTCATCACGATC
DIM-F	GCTTGTCTTCGCTTGCTAACG	bla_DIM	699
DIM-R	CGTTCGGCTGGATTGATTTG
KPC-Fm	CGTCTAGTTCTGCTGTCTTG	bla_KPC	798
KPC-Rm	CTTGTCATCCTTGTTAGGCG		232

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Table 2

- Characteristics of clinical specimens of patients with Pseudomonas aeruginosa infections.

Variables	CS PA (n=14)	MDR-PA (n=114)	CR-MDR-PA (n=161)	Total (N=289)
Gender
Male	10 (3.5)	70 (24.2)	98 (33.9)	178 (61.6)
Female	4 (1.4)	44 (15.2)	63 (21.8)	111 (38.4)
Underlying condition
Pulmonary disease	2 (0.7)	14 (4.8)	20 (6.9)	36 (12.5)
Gastrointestinal disease	1 (0.3)	14 (4.8)	16 (5.5)	31 (10.7)
Infectious disease	1 (0.3)	15 (5.2)	4 (1.4)	20 (6.9)
Malignancy	2 (0.7)	10 (3.5)	7 (2.4)	19 (6.6)
Neurologic disease	1 (0.3)	13 (4.5)	4 (1.4)	18 (6.2)
Genitourinary disease	1 (0.3)	7 (2.4)	8 (2.8)	16 (5.5)
Cardiovascular disease	2 (0.7)	9 (3.1)	5 (1.7)	16 (5.5)
Bone	0 (0.0)	9 (3.1)	7 (2.4)	16 (5.5)
Hematoma	0 (0.0)	8 (2.8)	4 (1.4)	12 (4.2)
Specimens
Sputum	11 (3.8)	70 (24.2)	78 (27.0)	159 (55.0)
Urine	2 (0.7)	10 (3.5)	44 (15.2)	56 (19.4)
Secretions*	0 (0.0)	8 (2.8)	15 (5.2)	23 (8.0)
Pus	0 (0.0)	8 (2.8)	8 (2.8)	16 (5.5)
Tissue	0 (0.0)	9 (3.1)	6 (2.1)	15 (5.2)
Blood	0 (0.0)	7 (2.4)	7 (2.4)	14 (4.8)
Catheter	1 (0.3)	2 (0.7)	3 (1.0)	6 (2.1)
ICU	3 (1.0)	22 (7.6)	26 (9.0)	51 (17.6)
Non-ICU	11 (3.8)	92 (31.8)	161 (46.7)	238 (82.4)
Hat Yai Hospital	2 (0.7)	7 (2.4)	79 (27.3)	88 (30.4)
Songklanagarind Hospital	12 (4.2)	107 (37.0)	82 (28.4)	201 (69.6)
Grouped by age
0-12 years	2 (0.7)	18 (6.2)	17 (5.9)	37 (12.8)
13-24 years	0 (0.0)	4 (1.4)	7 (2.4)	11 (3.8)
25-64 years	4 (1.4)	52 (18.0)	58 (20.1)	114 (39.4)
≥65 years	8 (2.8)	40 (13.8)	79 (27.3)	127 (43.9)

Values are presented as a number and precentage (%). *Penrose drain, bronchial wash, percutaneous nephrostomy, corneal ulcer, bile, and pleural fluid. CS-PA: carbapenem-susceptible Pseudomonas aeruginosa, MDR-PA: multidrug-resistant Pseudomonas aeruginosa, CR-MDR-PA: carbapenem-resistant multidrug-resistant Pseudomonas aeruginosa, ICU: intensive care unit

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Table 3

- Univariate analysis of risk factors for carbapenemase-encoding Pseudonomas aeruginosa infections.

Variables	Univariate analysis
Variables	MDR-PA/CS-PA	P-value	CR-MDR/CS-PA	P-value	MDR-PA/CR-MDR-PA	P-value
Gender
Male	0.636	0.515	0.349	0.133	0.549	0.078
Female
Underlying diseases
Pulmonary disease	3.261	0.302	5.174	0.149	1.587	0.499
Gastrointestinal disease	4.076	0.306	4.885	0.249	1.199	0.795
Infectious disease	7.375	0.169	2.839	0.495	0.385	0.247
Malignancy	1.304	0.829	1.088	0.947	0.834	0.813
Neurologic disease	6.583	0.162	1.865	0.66	0.283	0.136
Genitourinary disease	1.24	0.88	2.297	0.555	1.853	0.43
Cardiovascular disease	1.792	0.618	0.648	0.723	0.362	0.23
Bone	-	-	-	-	0.866	0.859
Hematoma	-	-	-	-	0.867	0.87
Specimens
Sputum	4.201	0.339	2.516	0.517	0.599	0.661
Urine	2.748	0.545	5.193	0.297	1.89	0.6
Secretions*	-	-	-	-	1.384	0.794
Pus	-	-	-	-	0.62	0.714
Tissue	-	-	-	-	0.713	0.792
Blood	-	-	-	-	0.464	0.563
Catheter
ICU	0.632	0.591	0.665	0.636	1.051	0.905
Non-ICU
Hat Yai Hospital	1.335	0.815	23.023	0.009	17.247	0
Songklanagarind Hospital
Age
0-12 years	1.742	0.608	0.497	0.519	0.285	0.023
13-24 years	-	-	-	-	0.544	0.44
25-64 years	2.172	0.282	0.671	0.584	0.309	0.002
≥65 years

Values are presented as an odds ratio (OR). *Penrose drain, bronchial wash, percutaneous nephrostomy, corneal ulcer, bile, and pleural fluid. CS-PA: carbapenem-susceptible Pseudonomas aeruginosa, MDR-PA: multidrug-resistant Pseudonomas aeruginosa, CR-MDR-PA: carbapenem-resistant multidrug-resistant Pseudonomas aeruginosa, ICU: intensive care unit

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Table 4

- Antimicrobial susceptibility among 289 clinical isolates of Pseudomonas aeruginosa.

Mode of action	Class	Antimicrobial agents	CS-MDR-PA (n=14)		MDR-PA (n=114)		CR-MDR-PA (n=161)		Total
Mode of action	Class	Antimicrobial agents	Sensitive	Resistant	Sensitive	Resistant	Sensitive	Resistant	Sensitive	Resistant
Protein synthesis (30S ribosomal subunit)	Aminoglycosides	Amikacin	11 (78.6)	2 (14.3)	99 (86.8)	11 (9.6)	1 (0.6)	128 (79.5)	111 (38.4)	141 (48.8)
	Aminoglycosides	Gentamicin	8 (57.1)	5 (35.7)	94 (82.5)	17 (14.9)	0 (0.0)	128 (79.5)	102 (35.3)	150 (51.9)
	β-lactams (cephalosporins), 3rd generation	Cefotaxime	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	6 (3.7)	0 (0.0)	6 (2.1)
		Ceftazidime	3 (21.4)	8 (57.1)	69 (60.5)	15 (13.2)	2 (1.2)	117 (72.7)	74 (25.6)	140 (48.4)
		Ceftriaxone	0 (0.0)	0 (0.0)	3 (2.6)	1 (0.9)	0 (0.0)	67 (41.6)	3 (1.0)	68 (23.5)
		Cefoperazone/sulbactam	5 (35.7)	3 (21.4)	66 (57.9)	21 (18.4)	18 (11.2)	102 (63.4)	89 (30.8)	126 (43.6)
Cell wall synthesis	β-lactams (carbapenem)	Imipenem	13 (92.9)	0 (0.0)	4 (3.5)	102 (89.5)	2 (1.2)	65 (40.4)	19 (6.6)	167 (57.8)
		Meropenem	13 (92.9)	0 (0.0)	21 (18.4)	76 (66.7)	0 (0.0)	67 (41.6)	34 (11.8)	143 (49.5)
		Ertapenem	1 (7.1)	0 (0.0)	0 (0.0)	2 (1.8)	0 (0.0)	31 (19.3)	1 (0.3)	33 (11.4)
	Combinations: piperacillin (β-lactams) and tazobactam (β-lactamase inhibitors)	Piperacillin/tazobactam	2 (14.3)	3 (21.4)	69 (60.5)	16 (14.0)	34 (21.1)	101 (62.7)	105 (36.3)	120 (41.5)
DNA gyrase	Fluoroquinolone	Levofloxacin	0 (0.0)	1 (7.1)	5 (4.4)	2 (1.8)	1 (0.6)	77 (47.8)	6 (2.1)	80 (27.7)
		Ciprofloxacin	7 (50.0)	4 (28.6)	81 (71.1)	26 (22.8)	0 (0.0)	61 (37.9)	88 (30.4)	91 (31.5)
		Norfloxacin	0 (0.0)	2 (14.3)	9 (7.9)	4 (3.5)	0 (0.0)	17 (10.6)	9 (3.1)	23 (8.0)
		Sitafloxacin	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	4 (2.5)	0 (0.0)	4 (1.4)
Cell membrane	Lipopeptides	Colistin	2 (14.3)	0 (0.0)	19 (16.7)	0 (0.0)	60 (37.3)	0 (0.0)	81 (28.0)	0 (0.0)

CS-MDR-PA: carbapenem-susceptible multidrug-resistant Pseudomonas aeruginosa, MDR-PA: multidrug-resistant Pseudomonas aeruginosa, CR-MDR-PA: carbapenem-resistant multidrug-resistant Pseudomonas aeruginosa