Research Article
Is Penicillin-Nonsusceptible Streptococcus pneumoniae a Significant Challenge to Healthcare System? A Systematic Review and Meta-Analysis
Table 1
Extracted information from eligible studies included in the meta-analysis.
| Author (ref) | Province | Published time | Enrollment time | Age group | Strain (n) | AST | Antibiotic resistance (n) | PNSP | ERY | AZM | TET | LVX | RIF | CLI | VAN | SXT | CHL | CRO | AMX | CIP | IPM | LZD | CTX | MDR |
| Gharibani et al. [8] | Ardabil | 2019 | 2015 | Children | 43 | Disk diffusion | 41 | 32 | 31 | 18 | 0 | 0 | 12 | 0 | 35 | 7 | ND | ND | ND | ND | ND | ND | 32 | Khoshdel et al. [9] | Chaharmahal and Bakhtiari | 2009 | 2007 | Children | 38 | Disk diffusion | 11 | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | Imani et al. [10] | Chaharmahal and Bakhtiari | 2007 | 2005 | ND | 17 | Broth microdilution | 16 | 10 | ND | ND | ND | ND | ND | ND | ND | ND | 1 | ND | 2 | ND | ND | ND | ND | Abdinia et al. [11] | East Azerbaijan | 2014 | 2003–2013 | Children | 37 | Disk diffusion | 14 | 6 | ND | ND | ND | 1 | ND | 0 | 12 | 2 | 4 | ND | 3 | ND | ND | 3 | ND | Hadi and Bagheri [12] | Fars | 2019 | 2011–2016 | Children | 10 | Disk diffusion | 7 | 3 | ND | ND | ND | ND | 3 | 0 | 9 | 1 | 4 | ND | ND | ND | ND | ND | ND | Kargar et al. [13] | Fars | 2015 | 2011–2012 | Children/adult | 45 | Disk diffusion | ND | ND | ND | ND | 31 | ND | ND | ND | ND | ND | ND | ND | 40 | ND | ND | ND | ND | Kargar et al. [14] | Fars | 2012 | 2010–2011 | Children/adult | 50 | Disk diffusion | 30 | 28 | 22 | 5 | 2 | ND | ND | ND | 24 | 0 | ND | ND | ND | ND | ND | 25 | 30 | Shishegar et al. [15] | Fars | 2011 | 2007–2008 | Children | 10 | Disk diffusion | ND | 1 | ND | ND | ND | ND | ND | ND | 10 | ND | 2 | 4 | 0 | ND | ND | 2 | ND | Japoni et al. [16] | Fars | 2010 | 2005–2006 | ND | 13 | Disk diffusion | 5 | 3 | ND | ND | ND | ND | 1 | 0 | 6 | 1 | ND | ND | 1 | ND | ND | ND | ND | Kohanteb and Sadeghi [17] | Fars | 2007 | ND | Children/adult | 115 | Broth microdilution | 39 | 21 | 15 | 28 | ND | ND | ND | 0 | ND | 9 | 7 | ND | 9 | ND | ND | 5 | ND | Ghaemi et al. [18] | Golestan | 2002 | 1998–1999 | Children | 63 | Disk diffusion | 35 | 5 | ND | 23 | ND | ND | 13 | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | Khademi et al. [19] | Hamadan | 2016 | 2013–2014 | Children/adult | 6 | Disk diffusion | ND | ND | ND | ND | ND | ND | ND | 0 | 3 | ND | 0 | ND | 1 | ND | ND | 0 | ND | Yousefi Mashouf et al. [20] | Hamadan | 2014 | 2009–2013 | Children | 35 | Disk diffusion | ND | ND | ND | ND | ND | ND | ND | ND | 9 | 12 | ND | 19 | ND | ND | ND | ND | ND | Yousefi Mashouf et al. [21] | Hamadan | 2003 | 1998–2000 | Children | 11 | Disk diffusion | ND | ND | ND | ND | ND | ND | ND | ND | 3 | 4 | ND | 6 | ND | ND | ND | ND | ND | Mosleh et al. [22, 23] | Hamadan | 2014 | ND | ND | 55 | E-test | 52 | 14 | 10 | ND | ND | ND | ND | 0 | ND | ND | ND | ND | 6 | 55 | ND | ND | 12 | Yeganeh-Moghadam et al. [24] | Isfahan | 2014 | 2011–2013 | Children | 15 | Disk diffusion | ND | 5 | 9 | ND | ND | ND | ND | ND | 15 | ND | 9 | 9 | 0 | ND | ND | 9 | ND | Ghazikalayeh et al. [25] | Isfahan | 2014 | 2011–2012 | Children | 291 | Disk diffusion | 47 | 10 | ND | 74 | 0 | 0 | 5 | 0 | ND | ND | ND | ND | ND | ND | 0 | ND | ND | Sabory et al. [26] | Kermanshah | 2015 | 2012 | Children | 83 | Disk diffusion | ND | ND | 53 | ND | ND | 34 | ND | ND | 31 | ND | 3 | 47 | ND | ND | ND | ND | 34 | Khosravi et al. [27] | Khuzestan | 2007 | 2005–2006 | Adult | 6 | Disk diffusion | ND | ND | ND | 3 | ND | ND | ND | ND | 0 | ND | 3 | ND | ND | ND | ND | ND | ND | Moafi and Issazadeh [28] | Qazvin | 2016 | 2013–2014 | Children | 6 | Disk diffusion | ND | ND | ND | ND | ND | ND | ND | ND | 4 | 4 | ND | ND | ND | ND | ND | ND | ND | Mamishi et al. [29] | Tehran | 2019 | 2017–2018 | Children | 4 | Disk diffusion | 1 | 4 | ND | ND | ND | ND | 2 | 0 | 1 | ND | ND | ND | ND | ND | ND | ND | ND | Ghahfarokhi et al. [30] | Tehran | 2020 | 2015–2019 | Children/adult | 80 | Disk diffusion | 29 | 49 | ND | 31 | ND | ND | 47 | 0 | 57 | 15 | 13 | ND | ND | ND | ND | ND | 41 | Azarsa et al. [31] | Tehran | 2019 | 2015 | Children/adult | 46 | Disk diffusion | 12 | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | Mousavi et al. [32] | Tehran | 2017 | 2014–2015 | Children | 76 | Disk diffusion | 76 | 65 | 65 | 4 | ND | 0 | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | 76 | Ahmadi et al. [33] | Tehran | 2019 | 2013–2016 | Children/adult | 100 | Disk diffusion | 22 | 59 | ND | 57 | ND | ND | 49 | ND | 92 | 23 | ND | ND | 3 | ND | ND | ND | 54 | Houri et al. [34] | Tehran | 2017 | 2013–2016 | Children | 53 | Broth microdilution | 11 | 15 | ND | 13 | 0 | ND | ND | 0 | 12 | ND | 4 | ND | ND | ND | 0 | 3 | 9 | Talebi et al. [35] | Tehran | 2019 | 2013–2015 | ND | 161 | Disk diffusion | 93 | 96 | ND | 121 | ND | ND | 84 | ND | 151 | 95 | ND | ND | ND | ND | ND | ND | 69 | Moghadam et al. [36] | Tehran | 2017 | 2013–2015 | Children/adult | 100 | Disk diffusion | 26 | 64 | ND | 77 | 0 | ND | 56 | 0 | 96 | 44 | 0 | ND | ND | 0 | 0 | ND | 71 | Farshad et al. [37] | Tehran | 2016 | 2013 | Adult | 48 | Disk diffusion | 40 | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | Rahbar et al. [38] | Tehran | 2019 | 2012–2016 | Children/adult | 50 | E-test | 15 | 36 | 35 | 28 | 1 | ND | 26 | 0 | 32 | 13 | ND | ND | ND | ND | ND | ND | ND | Tabatabaei et al. [39] | Tehran | 2017 | 2012–2015 | Children/adult | 73 | Broth microdilution | 16 | 61 | ND | ND | ND | ND | ND | 0 | 11 | ND | 23 | ND | ND | ND | ND | 31 | ND | Talebi et al. [40] | Tehran | 2016 | 2011–2013 | Children/adult | 100 | Disk diffusion | 28 | 60 | ND | 85 | ND | ND | 78 | 0 | 93 | 48 | 0 | 0 | ND | 0 | 0 | 0 | 50 | Azadegan et al. [41] | Tehran | 2015 | 2011–2013 | Children/adult | 186 | Disk diffusion | ND | 88 | ND | 186 | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | Abdollahi et al. [42] | Tehran | 2018 | 2011–2012 | Children | 102 | Disk diffusion | 61 | 24 | ND | 11 | 0 | ND | ND | 0 | 70 | 23 | ND | ND | ND | ND | ND | 0 | ND | Ahmadi et al. [43] | Tehran | 2013 | 2011 | Children/adult | 88 | Disk diffusion | ND | 47 | ND | 55 | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | Soltan Dallal et al. [44] | Tehran | 2013 | 2011 | Children/adult | 15 | Disk diffusion | 12 | 10 | ND | 0 | ND | ND | ND | 8 | ND | 8 | ND | 12 | ND | ND | ND | ND | ND | Sadeghi et al. [45] | Tehran | 2015 | 2010–2012 | Children/adult | 80 | E-test | 36 | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | Ahmadi et al. [46] | Tehran | 2015 | 2010–2012 | Children/adult | 70 | Disk diffusion | 60 | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | ND | Mahmoudi et al. [47] | Tehran | 2013 | 2009–2011 | Children | 7 | Disk diffusion | 5 | ND | ND | ND | ND | ND | ND | ND | 7 | ND | 4 | ND | ND | ND | ND | ND | ND | Khoramrooz et al. [48] | Tehran | 2012 | 2009–2010 | Children | 23 | Disk diffusion | 6 | 11 | 13 | ND | 0 | ND | 8 | 0 | 23 | ND | 3 | ND | 0 | ND | 0 | ND | ND | Rahimi et al. [49] | Tehran | 2015 | 2008–2012 | Children/adult | 38 | NA | 3 | 2 | ND | 8 | ND | ND | ND | 2 | 29 | 4 | ND | ND | 6 | ND | ND | ND | ND | Habibian et al. [50] | Tehran | 2013 | 2008–2012 | ND | 50 | Broth microdilution | 9 | ND | ND | ND | ND | ND | ND | 4 | ND | ND | ND | ND | 2 | ND | ND | ND | ND | Dashti et al. [51] | Tehran | 2012 | 2008–2009 | Children | 573 | Disk diffusion | 53 | ND | 315 | 377 | ND | 0 | ND | 9 | 68 | 34 | 26 | 23 | 9 | ND | ND | 17 | ND | Ashtiani et al. [52] | Tehran | 2014 | 2001–2011 | Children | 194 | Disk diffusion | 89 | 99 | ND | ND | ND | ND | ND | 0 | 139 | 58 | 23 | ND | ND | ND | ND | 25 | ND | Pourakbari et al. [53] | Tehran | 2012 | 2001–2005 | Children | 46 | Disk diffusion | 14 | 29 | ND | ND | ND | ND | 3 | ND | 38 | 8 | ND | ND | ND | ND | ND | ND | ND | Aligholi et al. [54] | Tehran | 2009 | 2001–2005 | Children | 50 | Agar dilution | 15 | 29 | ND | ND | ND | 0 | ND | 0 | ND | ND | 0 | ND | 15 | ND | ND | ND | ND | Oskoui et al. [55] | Tehran | 2010 | 2000–2008 | ND | 54 | Disk diffusion | 38 | 9 | ND | 10 | ND | ND | ND | ND | 28 | ND | ND | ND | ND | ND | ND | 2 | 9 | Jahanmehr et al. [56] | Tehran | 2004 | 1999–2001 | ND | 66 | Disk diffusion | 12 | ND | ND | ND | ND | ND | ND | 0 | ND | ND | ND | 12 | ND | ND | ND | ND | ND | Oskoui et al. [57] | Tehran | 2003 | 1998–2000 | ND | 130 | Disk diffusion | 114 | 10 | ND | 47 | ND | ND | ND | 0 | 57 | 28 | ND | ND | ND | ND | ND | ND | ND | Rezaeizadeh et al. [58] | Tehran | 2012 | 1998–2008 | Children | 30 | Disk diffusion | 17 | 6 | ND | ND | ND | ND | ND | 0 | 19 | 6 | ND | ND | ND | ND | ND | ND | ND | Modarres et al. [59] | Tehran | 1998 | 1993–1995 | Children | 51 | Disk diffusion | 1 | 1 | ND | ND | ND | ND | ND | 29 | 34 | 2 | ND | ND | ND | ND | ND | ND | ND | Gharailoo et al. [60] | Sistan and Balouchastan | 2016 | 2013–2014 | Children | 42 | Disk diffusion | 42 | 23 | ND | 26 | 0 | ND | ND | 0 | 39 | 6 | ND | 7 | ND | ND | ND | 0 | ND | Bokaeian et al. [61] | Sistan and Balouchastan | 2012 | 2008–2010 | Children | 75 | Disk diffusion | 62 | 66 | ND | 43 | 0 | ND | ND | 0 | 47 | 12 | 0 | ND | ND | 0 | ND | ND | 43 | Bokaeian et al. [62] | Sistan and Balouchastan | 2011 | 2007–2008 | Children/adult | 136 | Broth microdilution | 43 | 25 | ND | 13 | ND | ND | ND | 0 | ND | 11 | 5 | ND | 2 | ND | ND | 3 | 18 | Rahbar et al. [63] | West Azerbaijan | 2005 | 1999–2001 | ND | 24 | Disk diffusion | 8 | ND | ND | ND | ND | ND | 0 | 0 | 0 | ND | ND | ND | 0 | ND | ND | ND | ND | Behnaz et al. [64] | Yazd | 2004 | 2002 | Children | 72 | Disk diffusion | 36 | 45 | ND | 22 | ND | ND | ND | ND | 45 | ND | ND | ND | ND | ND | ND | ND | ND | Karami et al. [65] | Zanjan | 2009 | 2006–2007 | Children/adult | 57 | Broth macrodilution | 33 | ND | ND | ND | ND | ND | ND | 0 | ND | ND | ND | ND | ND | ND | ND | ND | ND |
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PNSP: penicillin-nonsusceptible S. pneumoniae (intermediately resistant and fully resistant); ERY: erythromycin; AZM: azithromycin; TET: tetracycline; LVX: levofloxacin; RIF: rifampin; CLI: clindamycin; VAN: vancomycin; SXT: trimethoprim/sulfamethoxazole; CHL: chloramphenicol; CRO: ceftriaxone; AMX: amoxicillin; CIP: ciprofloxacin; IPM: imipenem; LZD: linezolid; CTX: cefotaxime; MDR: multidrug-resistant (resistant to ≥3 antibiotic classes); AST: antimicrobial susceptibility testing; ND: not determined.
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