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. 2018 Oct 17;11:1831–1880. doi: 10.2147/IDR.S176049

Table 2.

Studies that considered phenotypic methods for detecting carbapenemase enzymes

Author (year) Setting Population Samples Microorganism (no.) MICa Method of carbapenemase detection Resistance to FQ and AG Resultsb Weak points Strength points

Ghotaslou et al (2018)26 Five hospitals in East and West Azerbaijan General inpatients Different sites Enterobacteriaceae (307) • DD
• BA and DPA for MBL detection
c • Resistance rate to carbapenem was observed only in K. pneumonia (57 isolates; 25%–45%)
• Of these 57 isolates, phenotypic methods revealed that 15%, 7%, and 3% isolates of Klebsiella had MBL, KPC, and OXA-48 genes, respectively
• Most of the carbapenemase strains were isolated from urine and blood
• Small sample size for each species
Saadatian Farivar et al (2018)27 Three hospitals in Tehran Inpatients and outpatients Different sites Klebsiella pneumonia (81) • DD
• MHT for MBL detection
OFX 65%, CIP 68%, NOR 66%, GEN 66%, AMK 51%, TOB 56 %, KAN 79%, GEN 96% • Resistance rate to IPM was 45%
• 6 (7.4% of all) isolates were positive for MHT test
Moosavian et al (2014)28 Two hospitals in Ahvaz General inpatients Different sites Acinetobacter spp. (100) • DD
• MHT
AMK 96% CIP 98% • Resistance rates to IPM, MEM, and ERT were 95%, 96%, and 53%, respectively
• 53% of all strains were MHT positive
Jonaidi Jafari et al (2014)29 One hospital in Tehran General inpatients Different sites Different strains (350) • DD
• CDT for ESBL detection
• MIC was determined by E-test
• 95 strains were ESBLs
• Resistance rates to IPM and MEM according to MIC, respectively, were: Acinetobacter baumannii 42%, 37% Pseudomonas aeruginosa 42%, 60% K. pneumonia 15%, 0%
• Small sample size for each microorganism
Ghadiri et al (2014)30 Three laboratories in Tehran General outpatients Urine Escherichia coli (300) • DD
• CDT for ESBL detection
• DDST for MBL detection
AMK 11%
GEN 16%
• 67 isolates were ESBL producers and resistance to carbapenem in this group was about 10%
• 21 isolates were MBL producers and resistance to carbapenems among them was almost 100%
• 5 isolates were both MBL and ESBL positive
• Large sample size
Fazeli et al (2014)31 Teaching hospitals in Isfahan General inpatients and ICU patients Different sites K. pneumonia (142) • DD
• CDT for ESBL
Resistance rate to GEN and AMK and CIP: 70%–80% LVX: 50%–60% • Resistance rates to IPM, MEM, and ERT among all strains were 57%, 52%, and 47%, respectively
• 101 strains were ESBL producers
• Most of the ESBL producers were isolated from ICU and from urine samples
• It is not clear that the study was multicenter or not
Mirsalehian et al (2014)32 Motahari hospital Burn patients Probably burn wounds P. aeruginosa (100) • DD
• AmpC disk and CDT for AmpC production
• All IPM-resistant Pseudomonas were chosen and mean MIC for IPM was 64 mcg/mL
• AmpC disk test and CDT were positive for 54 and 17 isolates, respectively showing a probable activation of one of the efflux pump and impermeability systems, or both
Moayednia et al (2014)33 One hospital in Isfahan General inpatients and outpatients Urine K. pneumonia (484) and E. coli (1,080) • DD
• Double Disk for ESBL
• MHT for KPC detection
• CDT for MBL detection
Just reported for ESBL producer • Resistance rate to carbapenem for E. coli was 1%–2% and for Klebsiella spp., it was 41%–46%
• 390 isolates of E. coli and 238 Klebsiella were ESBL producers
• From all of strains: E. coli: 2 MBL and 10 KPC producers Klebsiella spp.: 10 MBL and 186 KPC producers
• MIC was done by E-test, but cutoffs were not reported • Large sample size
Erfani et al (2013)34 Three hospitals in Tehran General inpatients Different sites Acinetobacter sp. (107) • DD
• CDT for MBL detection
CIP 95%
LVX 93%
GEN 51%
TOB 64%
• Resistance rate to IPM and MEM was about 95% and 92% of these resistant isolates were MBL positive
Lari et al (2013)24 One hospital in Tehran (Motahhari) Burn patients Mostly burn wound Acinetobacter spp. (69) • SDDT for ESBL detection
• CDT for MBL detection
GEN 64.7%
AMK 95.7%
KAN 97.1%
TOB 2.9%
CIP 97.1%
• Resistance rate to IPM was 92% • ESBL was positive in 10% of isolates
• 24% of all baumannii isolates were MBL positive
• The mortality rate in this study was 20%
• Mortality rate was reported
• Detection of Integron genes
Rastegar Lari et al (2013)25 One hospital in Tehran (Motahari) Burn patients Burn wounds Klebsiella spp. (35) • DD
• MHT for KPC production
AMK 71%
GEN 72%
TOB 86%
• Resistance rate to IPM was 54% and all were KPC producers
• 7 out of 28 patients had two Klebsiella isolates with two different antibiotypes
• Rate of mortality in patients infected with resistant strain was 33%
• FQ and colistin were not tested
• MIC values were not reported
• Small sample size
• Mortality rate was reported
Safari et al (2013)35 Three educational hospitals in Hamadan ICU patients Trachea, blood, urine, sputum, wounds A. baumannii (100) • DD
• E-test for MBL
Resistant: CIP 97%
LVX 91%
AMK 84%
GEN 88%
• Resistance rate to carbapenem was 85%–94% but according to MIC, it was 87%–99%
• 99% of all isolates were MBL producers
• Multicenter study
• MIC was reported
Masaeli et al (2012)36 Two hospitals in Sanandaj General inpatients Different sites Different strains (423) • DD
• DDST for MBL detection
GEN 70%
AMK 80%
CIP 37%
NOR 42%
• The result of disk diffusion for carbapenem was not reported
• 126 isolates (30% of all) were MBL positive
• Risk factors like immunosuppression and use of antibiotics during the past 2 weeks were correlated with infection by MBL producers
• The resistance pattern of each group of microorganisms was not fully defined • Correlation between being MBL and different clinical risk factors was assessed
Japoni-Nejad et al (2013)37 One hospital in Arak General inpatients and environmental isolates Different strains A. baumannii (63) • MHT for KPC detection
• E-test
Amikacin 80%
Netilmicin 54%
• 84% were resistant to carbapenem
• 47 isolates were MBL producers according to E-test and three of them were MHT positive
• 60 strains had MIC more than 256
• Isolates from environment of hospital were also included • Small sample size
Haji Hashemi et al (2012)39 Different hospitals in Tehran and Isfahan General inpatients and outpatients Different sites Klebsiella pneumoniae (244) • DD
• MHT for KPC detection
• CHROMagar for KPC detection
• MHT and CHROMagar were compared
• From all, 30 and 36 isolates were KPC producers according to MHT and CHROMagar, respectively. The infection of burn wounds at the highest percentage: 27 cases (75 %)
• MIC was not reported • Multicenter study
Azimi et al (2012)40 Two burn hospitals in Tehran Infant and pediatric patients Not defined (probably burn wounds) Klebsiella, Acinetobacter, and Pseudomonas (64 strains from 20 patients) • DD
• MHT for KPC production
• CDT for ESBL detection
Not defined • 36 isolates were resistant to all tested antibiotic (not mentioned which antibiotics) except Colistin
• Among these 36 isolates, 15 isolates were resistant to IPM
• From these 15 isolates, 13 were KPC and 6 were ESBL producers
• Types of samples were not defined
• The sample size is very small (7 A. baumannii, 16 Enterobacteriaceae, 12 Pseudomonas)
• There is no precise data of resistance to each antibiotic
Japoni et al (2006)41 One hospital in Shiraz General inpatients Different sites (mostly wound) P. aeruginosa (70) • DD
• DDST for ESBL
• MHT for MBL detection
CIP 73%
AMK 93%
TOB 97%
• Resistance rate to carbapenems was 33%
• MIC value for IPM was 2 and for MEM was 1
• MBL was not detected
• Small sample size

Notes:

a

MIC values for carbapenems (but not other antimicrobial agents) were determined.

b

Resistance rates were according to the result of disk diffusion test.

c

For complete information about the resistance to AG and FQ, please refer to the original reference.

Abbreviations: AG, aminoglycoside; AMK, amikacin; BA, boronic acid; CDT, combination disk test; CIP, ciprofloxacin; DD, disk diffusion; DDST, double disk synergy test; DOR, doripenem; DPA, dipicolinic acid; ERT, ertapenem; ESBL, extended spectrum β-lactamase; FQ, fluoroquinolones; GEN, gentamicin; ICU, intensive care unit; IPM, imipenem; KAN, kanamycin; KPC, Klebsiella-producing carbapenemase; LVX, levofloxacin; MBL, metallo-β-lactamase; MEM, meropenem; MHT, modified Hodge test; MIC, minimum inhibitory concentration; NAL, nalidixic acid; NOR, norfloxacin; OFX, ofloxacin; TOB, tobramycin.