A five-year systematic review and meta-analysis study on methicillin resistant Staphylococcus epidermidis strains in Iran
Abstract
Background and Objectives: One of the most prevalent drug-resistant bacteria is methicillin-resistant Staphylococcus epidermidis (MRSE) causing healthcare infections. Previously, a meta-analysis study on the frequency of MRSE was conducted from Mar 2006 to Jan 2016 in Iran. The present study aimed to evaluate the changes in this prevalence in the last 5 years in different cities in Iran.
Materials and Methods: Published articles on the frequency of MRSE were collected from the Web of Science, PubMed, Scopus, Google Scholar, Cochrane Library, and Iranian databases from the beginning of 2016 to the end of 2020. Of the 503 records identified, 17 studies met the inclusion criteria, and their extracted data were analyzed using comprehensive meta-analysis version 2.0 (Biostat).
Results: The analysis showed that the frequency of MRSE has decreased significantly in the last five years and reached 60.8 [95% confidence interval (95% CI) 54.2-66.9] among culture-positive cases of S. epidermidis in Iran.
Conclusion: The noticeable reduction in the prevalence of MRSE in Iran could be due to the improvement of infection control programs and interruption of the pathogen transmission cycle. Another influential reason is the significant reduction in methicillin prescriptions by physicians for infections caused by staphylococci.
1. Nguyen TH, Park MD, Otto M. Host Response to Staphylococcus epidermidis colonization and infections. Front Cell Infect Microbiol 2017; 7: 90.
2. Kalani BS, Khodaei F, Moghadampour M, Lotfollahi L, Ohadi E, Foroozeshfard M, et al. TRs analysis revealed Staphylococcus epidermidis transmission among patients and hospital. Ann Ig 2019; 31: 52-61.
3. Van Cauter M, Cornu O, Yombi J-C, Rodriguez-Villalobos H, Kaminski L. The effect of storage delay and storage temperature on orthopaedic surgical samples contaminated by Staphylococcus epidermidis. PLoS One 2018; 13(3): e0192048.
4. Otto M. Staphylococcus epidermidis pathogenesis. Methods Mol Biol 2014; 1106: 17-31.
5. Otto M. Staphylococcus epidermidis--the “accidental” pathogen. Nat Rev Microbiol 2009; 7: 555-567.
6. Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin Microbiol Rev 2014; 27: 870-926.
7. Yeranosian MG, Arshi A, Terrell RD, Wang JC, McAllister DR, Petrigliano FA. Incidence of acute postoperative infections requiring reoperation after arthroscopic shoulder surgery. Am J Sports Med 2014; 42: 437-441.
8. Carbon C. MRSA and MRSE: Is there an answer. Clin Microbiol Infect 2000; 6 Suppl 2: 17-22.
9. Razavi S, Dadashi M, Pormohammad A, Khoramrooz SS, Mirzaii M, Gholipour A, et al. Methicillin-resistant Staphylococcus epidermidis in Iran: A systematic review and meta-analysis. Arch Clin Infect Dis 2018; 13(4): e58410.
10. Nasiri MJ, Imani Fooladi AA, Dabiri H, Pormohammad A, Salimi Chirani A, Dadashi M, et al. Primary ethambutol resistance among Iranian pulmonary tuberculosis patients: a systematic review. Ther Adv Infect Dis 2016; 3: 133-138.
11. Houri H, Pormohammad A, Riahi SM, Nasiri MJ, Fallah F, Dabiri H, et al. Acute bacterial meningitis in Iran: Systematic review and meta-analysis. PLoS One 2017; 12(2): e0169617.
12. Munn Z, Moola S, Riitano D, Lisy K. The development of a critical appraisal tool for use in systematic reviews addressing questions of prevalence. Int J Health Policy Manag 2014; 3: 123-128.
13. Abbasi Montazeri E, Seyed-Mohammadi S, Asarehzadegan Dezfuli A, Khosravi AD, Dastoorpoor M, Roointan M, et al. Investigation of SCCmec types I–IV in clinical isolates of methicillin-resistant coagulase-negative staphylococci in Ahvaz, Southwest Iran. Biosci Rep 2020; 40: BSR20200847.
14. Behshood P, Tajbakhsh E, Momtaz H. Recognition of (Sesc) for easy identification of Staphylococcus epidermidis and molecular and phenotypic study of Β-Lactam resistance in Staphylococcus epidermidis isolates in Isfahan. Rep Biochem Mol Biol 2020; 9: 309-314.
15. Nasaj M, Saeidi Z, Asghari B, Roshanaei G, Arabestani MR. Identification of hemolysin encoding genes and their association with antimicrobial resistance pattern among clinical isolates of coagulase-negative Staphylococci. BMC Res Notes 2020; 13: 68.
16. Mamishi S, Mohammadian M, Pourakbari B, Hosseinpour Sadeghi R, Ashtiani MTH, Abdosalehi MR, et al. Antibiotic resistance and genotyping of Gram-positive bacteria causing hospital-acquired infection in patients referring to children’s medical center. Infect Drug Resist 2019; 12: 3719-3726.
17. Borooni S, Nourbakhsh V, Nourbakhsh F, Tajbakhsh E, Yazdanpanah A. Biofilm formation and its genes expressions in Staphylococcus epidermidis isolated from urinary tract infections of children in Isfahan. Int Arch Health Sci 2019; 6: 41-45.
18. Chabi R, Momtaz H. Virulence factors and antibiotic resistance properties of the Staphylococcus epidermidis strains isolated from hospital infections in Ahvaz, Iran. Trop Med Health 2019; 47: 56.
19. Ghaznavi-Rad E, Fard-Mousavi N, Shahsavari A, Japoni-Nejad A, Van Belkum A. Distribution of staphylococcal cassette chromosome mec types among methicillin-resistant coagulase negative staphylococci in central Iran. Iran J Microbiol 2018; 10: 7-13.
20. Behrooz SK, Lida L, Ali S, Mehdi M, Rasoul M, Elnaz O, et al. Study of MAZEF, SAM, and PHD-DOC putative toxin-antitoxin systems in Staphylococcus epidermidis. Acta Microbiol Immunol Hung 2018; 65: 81-91.
21. Tahmasebi H, Dehbashi S, Arabestani MR. Determination of antimicrobial resistance pattern in methicillin-resistant Staphylococcus saprophyticus and Staphylococcus epidermidis and detection of resistance Genes to clindamycin and Erythromycin. Iran J Med Microbiol 2018; 12: 169-178.
22. Sharifinejad M, Shokatpour N, Farnaghi F, Abedinyfar Z, Amoli FA, Doustdar F. Different genotypes of adhesion operon genes in Staphylococcus epidermidis isolates from various ocular infections. Eye Contact Lens 2018; 44 Suppl 2: S277-S280.
23. Halaji M, Karimi A, Shoaei P, Nahaei M, Khorvash F, Ataei B, et al. Distribution of SCCmec elements and presence of Panton-Valentine Leukocidin in methicillin-resistant Staphylococcus epidermidis isolated from clinical samples in a University Hospital of Isfahan city, Iran. J Clin Diagn Res 2017; 11: DC27-DC31.
24. Ebrahimzadeh Namvar A, Havaei SA, Douraghi M. Molecular Characterization of Staphylococcus epidermidis isolates recovered from patients admitted to a referral Hospital in Iran. Arch Clin Infect Dis 2017; 12(2): e38675.
25. Soroush S, Jabalameli F, Taherikalani M, Amirmozafari N, Fooladi AAI, Asadollahi K, et al. Investigation of biofilm formation ability, antimicrobial resistance and the staphylococcal cassette chromosome mec patterns of methicillin resistant Staphylococcus epidermidis with different sequence types isolated from children. Microb Pathog 2016; 93: 126-130.
26. Mirzaei R, Talebi M, Mahdiun F, Foroozeshfard M, Irajian G. Discrimination between invasive and contaminating Staphylococcus epidermidis strains according to the multiplex-PCR and study of phenotypic drug resistance. Iran J Med Microbiol 2017; 10: 9-15.
27. Saffari F, Widerström M, Gurram BK, Edebro H, Hojabri Z, Monsen T. Molecular and phenotypic characterization of multidrug-resistant clones of Staphylococcus epidermidis in Iranian Hospitals: Clonal relatedness to healthcare-associated methicillin-resistant isolates in Northern Europe. Microb Drug Resist 2016; 22: 570-577.
28. Tahmasebi H, Bokaeian M, Adabi J. Phenotypic and molecular study of beta-lactam resistance in coagulasenegative staphylococci samples. Pars J Med Sci 2016; 14: 55-63.
29. Vicetti Miguel CP, Mejias A, Leber A, Sanchez PJ. A decade of antimicrobial resistance in Staphylococcus aureus: A single center experience. PLoS One 2019; 14(2): e0212029.
30. Kramer TS, Schröder C, Behnke M, Aghdassi SJ, Geffers C, Gastmeier P, et al. Decrease of methicillin resistance in Staphylococcus aureus in nosocomial infections in Germany–a prospective analysis over 10 years. J Infect 2019; 78: 215-219.
31. Walter J, Noll I, Feig M, Weiss B, Claus H, Werner G, et al. Decline in the proportion of methicillin resistance among Staphylococcus aureus isolates from non-invasive samples and in outpatient settings, and changes in the co-resistance profiles: An analysis of data collected within the Antimicrobial Resistance Surveillance Network, Germany 2010 to 2015. BMC Infect Dis 2017; 17: 169.
32. Rosdahl VT, Knudsen AM. The decline of methicillin resistance among Danish Staphylococcus aureus strains. Infect Control Hosp Epidemiol 1991; 12: 83-88.
33. Kardas-Słoma L, Boëlle P-Y, Opatowski L, Guillemot D, Temime L. Antibiotic reduction campaigns do not necessarily decrease bacterial resistance: The example of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2013; 57: 4410-4416.
34. Bruinsma N, Hutchinson JM, van den Bogaard AE, Giamarellou H, Degener J, Stobberingh EE. Influence of population density on antibiotic resistance. J Antimicrob Chemother 2003; 51: 385-390.
35. Pronovost P, Needham D, Berenholtz S, Sinopoli D, Chu H, Cosgrove S, et al. An intervention to decrease catheter-related bloodstream infections in the ICU. N Engl J Med 2006; 355: 2725-2732.
36. Centers for Disease Control and Prevention (CDC). Reduction in central line--associated bloodstream infections among patients in intensive care units --- Pennsylvania, April 2001--March 2005. MMWR Morb Mortal Wkly Rep 2005; 54: 1013-1016.
37. Centers for Disease Control and Prevention (CDC). Vital Signs: Central Line--Associated Blood Stream Infections --- United States, 2001, 2008, and 2009. MMWR Morb Mortal Wkly Rep 2011; 60: 243-248.
38. Perlin JB, Hickok JD, Septimus EJ, Moody JA, Englebright JD, Bracken RM. A bundled approach to reduce methicillin-resistant Staphylococcus aureus infections in a system of community hospitals. J Healthc Qual 2013; 35: 57-68.
39. Jain R, Kralovic SM, Evans ME, Ambrose M, Simbartl LA, Obrosky DS, et al. Veterans affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections. N Engl J Med 2011; 364: 1419-1430.
40. Landrum ML, Neumann C, Cook C, Chukwuma U, Ellis MW, Hospenthal DR, et al. Epidemiology of Staphylococcus aureus blood and skin and soft tissue infections in the US Military Health System, 2005-2010. JAMA 2012; 308: 50-59.
41. Dantes R, Mu Y, Belflower R, Aragon D, Dumyati G, Harrison LH, et al. National burden of invasive methicillin-resistant Staphylococcus aureus infections, United States, 2011. JAMA Intern Med 2013; 173: 1970-1978.
42. Burton DC, Edwards JR, Horan TC, Jernigan JA, Fridkin SK. Methicillin-resistant Staphylococcus aureus central line-associated bloodstream infections in US intensive care units, 1997-2007. JAMA 2009; 301: 727-736.
43. Sutter DE, Milburn E, Chukwuma U, Dzialowy N, Maranich AM, Hospenthal DR. Changing susceptibility of Staphylococcus aureus in a US pediatric population. Pediatrics 2016; 137(4):e20153099.
44. Kaplan SL. Staphylococcus aureus infections in children: The implications of changing trends. Pediatrics 2016; 137(4): e20160101.
45. Wisplinghoff H, Rosato AE, Enright MC, Noto M, Craig W, Archer GL. Related clones containing SCCmec Type IV predominate among clinically significant Staphylococcus epidermidis isolates. Antimicrob Agents Chemother 2003; 47: 3574-3579.
46. Hiramatsu K, Cui L, Kuroda M, Ito T. The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 2001; 9: 486-493.
47. Iravani Mohammad Abadi M, Moniri R, Khorshidi A, Piroozmand A, Mousavi SGA, Dastehgoli K, et al. Molecular characteristics of nasal carriage methicillin-resistant coagulase negative staphylococci in school students. Jundishapur J Microbiol 2015; 8(6): e18591.
48. Miragaia M, Couto I, De Lencastre H. Genetic diversity among methicillin-resistant Staphylococcus epidermidis (MRSE). Microb Drug Resist 2005; 11: 83-93.
49. Ibrahem S, Salmenlinna S, Virolainen A, Kerttula A-M, Lyytikainen O, Jägerroos H, et al. Carriage of methicillin-resistant staphylococci and their SCCmec types in a long-term-care facility. J Clin Microbiol 2009; 47: 32-37.
50. Streit JM, Jones RN, Sader HS, Fritsche TR. Assessment of pathogen occurrences and resistance profiles among infected patients in the intensive care unit: Report from the SENTRY Antimicrobial Surveillance Program (North America, 2001). Int J Antimicrob Agents 2004; 24: 111-118.
51. Weinstein RA. Controlling antimicrobial resistance in hospitals: Infection control and use of antibiotics. Emerg Infect Dis 2001; 7: 188-192.
52. Piette A, Verschraegen G. Role of coagulase-negative staphylococci in human disease. Vet Microbiol 2009; 134: 45-54.
53. Anvari MS, Kianinejad R, Ali Boroumand M, Arzhan S, Jalali A. Bacterial pericarditis and antimicrobial resistance at the Tehran heart center, Iran. J Infect Dev Ctries 2015; 9: 780-784.
2. Kalani BS, Khodaei F, Moghadampour M, Lotfollahi L, Ohadi E, Foroozeshfard M, et al. TRs analysis revealed Staphylococcus epidermidis transmission among patients and hospital. Ann Ig 2019; 31: 52-61.
3. Van Cauter M, Cornu O, Yombi J-C, Rodriguez-Villalobos H, Kaminski L. The effect of storage delay and storage temperature on orthopaedic surgical samples contaminated by Staphylococcus epidermidis. PLoS One 2018; 13(3): e0192048.
4. Otto M. Staphylococcus epidermidis pathogenesis. Methods Mol Biol 2014; 1106: 17-31.
5. Otto M. Staphylococcus epidermidis--the “accidental” pathogen. Nat Rev Microbiol 2009; 7: 555-567.
6. Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin Microbiol Rev 2014; 27: 870-926.
7. Yeranosian MG, Arshi A, Terrell RD, Wang JC, McAllister DR, Petrigliano FA. Incidence of acute postoperative infections requiring reoperation after arthroscopic shoulder surgery. Am J Sports Med 2014; 42: 437-441.
8. Carbon C. MRSA and MRSE: Is there an answer. Clin Microbiol Infect 2000; 6 Suppl 2: 17-22.
9. Razavi S, Dadashi M, Pormohammad A, Khoramrooz SS, Mirzaii M, Gholipour A, et al. Methicillin-resistant Staphylococcus epidermidis in Iran: A systematic review and meta-analysis. Arch Clin Infect Dis 2018; 13(4): e58410.
10. Nasiri MJ, Imani Fooladi AA, Dabiri H, Pormohammad A, Salimi Chirani A, Dadashi M, et al. Primary ethambutol resistance among Iranian pulmonary tuberculosis patients: a systematic review. Ther Adv Infect Dis 2016; 3: 133-138.
11. Houri H, Pormohammad A, Riahi SM, Nasiri MJ, Fallah F, Dabiri H, et al. Acute bacterial meningitis in Iran: Systematic review and meta-analysis. PLoS One 2017; 12(2): e0169617.
12. Munn Z, Moola S, Riitano D, Lisy K. The development of a critical appraisal tool for use in systematic reviews addressing questions of prevalence. Int J Health Policy Manag 2014; 3: 123-128.
13. Abbasi Montazeri E, Seyed-Mohammadi S, Asarehzadegan Dezfuli A, Khosravi AD, Dastoorpoor M, Roointan M, et al. Investigation of SCCmec types I–IV in clinical isolates of methicillin-resistant coagulase-negative staphylococci in Ahvaz, Southwest Iran. Biosci Rep 2020; 40: BSR20200847.
14. Behshood P, Tajbakhsh E, Momtaz H. Recognition of (Sesc) for easy identification of Staphylococcus epidermidis and molecular and phenotypic study of Β-Lactam resistance in Staphylococcus epidermidis isolates in Isfahan. Rep Biochem Mol Biol 2020; 9: 309-314.
15. Nasaj M, Saeidi Z, Asghari B, Roshanaei G, Arabestani MR. Identification of hemolysin encoding genes and their association with antimicrobial resistance pattern among clinical isolates of coagulase-negative Staphylococci. BMC Res Notes 2020; 13: 68.
16. Mamishi S, Mohammadian M, Pourakbari B, Hosseinpour Sadeghi R, Ashtiani MTH, Abdosalehi MR, et al. Antibiotic resistance and genotyping of Gram-positive bacteria causing hospital-acquired infection in patients referring to children’s medical center. Infect Drug Resist 2019; 12: 3719-3726.
17. Borooni S, Nourbakhsh V, Nourbakhsh F, Tajbakhsh E, Yazdanpanah A. Biofilm formation and its genes expressions in Staphylococcus epidermidis isolated from urinary tract infections of children in Isfahan. Int Arch Health Sci 2019; 6: 41-45.
18. Chabi R, Momtaz H. Virulence factors and antibiotic resistance properties of the Staphylococcus epidermidis strains isolated from hospital infections in Ahvaz, Iran. Trop Med Health 2019; 47: 56.
19. Ghaznavi-Rad E, Fard-Mousavi N, Shahsavari A, Japoni-Nejad A, Van Belkum A. Distribution of staphylococcal cassette chromosome mec types among methicillin-resistant coagulase negative staphylococci in central Iran. Iran J Microbiol 2018; 10: 7-13.
20. Behrooz SK, Lida L, Ali S, Mehdi M, Rasoul M, Elnaz O, et al. Study of MAZEF, SAM, and PHD-DOC putative toxin-antitoxin systems in Staphylococcus epidermidis. Acta Microbiol Immunol Hung 2018; 65: 81-91.
21. Tahmasebi H, Dehbashi S, Arabestani MR. Determination of antimicrobial resistance pattern in methicillin-resistant Staphylococcus saprophyticus and Staphylococcus epidermidis and detection of resistance Genes to clindamycin and Erythromycin. Iran J Med Microbiol 2018; 12: 169-178.
22. Sharifinejad M, Shokatpour N, Farnaghi F, Abedinyfar Z, Amoli FA, Doustdar F. Different genotypes of adhesion operon genes in Staphylococcus epidermidis isolates from various ocular infections. Eye Contact Lens 2018; 44 Suppl 2: S277-S280.
23. Halaji M, Karimi A, Shoaei P, Nahaei M, Khorvash F, Ataei B, et al. Distribution of SCCmec elements and presence of Panton-Valentine Leukocidin in methicillin-resistant Staphylococcus epidermidis isolated from clinical samples in a University Hospital of Isfahan city, Iran. J Clin Diagn Res 2017; 11: DC27-DC31.
24. Ebrahimzadeh Namvar A, Havaei SA, Douraghi M. Molecular Characterization of Staphylococcus epidermidis isolates recovered from patients admitted to a referral Hospital in Iran. Arch Clin Infect Dis 2017; 12(2): e38675.
25. Soroush S, Jabalameli F, Taherikalani M, Amirmozafari N, Fooladi AAI, Asadollahi K, et al. Investigation of biofilm formation ability, antimicrobial resistance and the staphylococcal cassette chromosome mec patterns of methicillin resistant Staphylococcus epidermidis with different sequence types isolated from children. Microb Pathog 2016; 93: 126-130.
26. Mirzaei R, Talebi M, Mahdiun F, Foroozeshfard M, Irajian G. Discrimination between invasive and contaminating Staphylococcus epidermidis strains according to the multiplex-PCR and study of phenotypic drug resistance. Iran J Med Microbiol 2017; 10: 9-15.
27. Saffari F, Widerström M, Gurram BK, Edebro H, Hojabri Z, Monsen T. Molecular and phenotypic characterization of multidrug-resistant clones of Staphylococcus epidermidis in Iranian Hospitals: Clonal relatedness to healthcare-associated methicillin-resistant isolates in Northern Europe. Microb Drug Resist 2016; 22: 570-577.
28. Tahmasebi H, Bokaeian M, Adabi J. Phenotypic and molecular study of beta-lactam resistance in coagulasenegative staphylococci samples. Pars J Med Sci 2016; 14: 55-63.
29. Vicetti Miguel CP, Mejias A, Leber A, Sanchez PJ. A decade of antimicrobial resistance in Staphylococcus aureus: A single center experience. PLoS One 2019; 14(2): e0212029.
30. Kramer TS, Schröder C, Behnke M, Aghdassi SJ, Geffers C, Gastmeier P, et al. Decrease of methicillin resistance in Staphylococcus aureus in nosocomial infections in Germany–a prospective analysis over 10 years. J Infect 2019; 78: 215-219.
31. Walter J, Noll I, Feig M, Weiss B, Claus H, Werner G, et al. Decline in the proportion of methicillin resistance among Staphylococcus aureus isolates from non-invasive samples and in outpatient settings, and changes in the co-resistance profiles: An analysis of data collected within the Antimicrobial Resistance Surveillance Network, Germany 2010 to 2015. BMC Infect Dis 2017; 17: 169.
32. Rosdahl VT, Knudsen AM. The decline of methicillin resistance among Danish Staphylococcus aureus strains. Infect Control Hosp Epidemiol 1991; 12: 83-88.
33. Kardas-Słoma L, Boëlle P-Y, Opatowski L, Guillemot D, Temime L. Antibiotic reduction campaigns do not necessarily decrease bacterial resistance: The example of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2013; 57: 4410-4416.
34. Bruinsma N, Hutchinson JM, van den Bogaard AE, Giamarellou H, Degener J, Stobberingh EE. Influence of population density on antibiotic resistance. J Antimicrob Chemother 2003; 51: 385-390.
35. Pronovost P, Needham D, Berenholtz S, Sinopoli D, Chu H, Cosgrove S, et al. An intervention to decrease catheter-related bloodstream infections in the ICU. N Engl J Med 2006; 355: 2725-2732.
36. Centers for Disease Control and Prevention (CDC). Reduction in central line--associated bloodstream infections among patients in intensive care units --- Pennsylvania, April 2001--March 2005. MMWR Morb Mortal Wkly Rep 2005; 54: 1013-1016.
37. Centers for Disease Control and Prevention (CDC). Vital Signs: Central Line--Associated Blood Stream Infections --- United States, 2001, 2008, and 2009. MMWR Morb Mortal Wkly Rep 2011; 60: 243-248.
38. Perlin JB, Hickok JD, Septimus EJ, Moody JA, Englebright JD, Bracken RM. A bundled approach to reduce methicillin-resistant Staphylococcus aureus infections in a system of community hospitals. J Healthc Qual 2013; 35: 57-68.
39. Jain R, Kralovic SM, Evans ME, Ambrose M, Simbartl LA, Obrosky DS, et al. Veterans affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections. N Engl J Med 2011; 364: 1419-1430.
40. Landrum ML, Neumann C, Cook C, Chukwuma U, Ellis MW, Hospenthal DR, et al. Epidemiology of Staphylococcus aureus blood and skin and soft tissue infections in the US Military Health System, 2005-2010. JAMA 2012; 308: 50-59.
41. Dantes R, Mu Y, Belflower R, Aragon D, Dumyati G, Harrison LH, et al. National burden of invasive methicillin-resistant Staphylococcus aureus infections, United States, 2011. JAMA Intern Med 2013; 173: 1970-1978.
42. Burton DC, Edwards JR, Horan TC, Jernigan JA, Fridkin SK. Methicillin-resistant Staphylococcus aureus central line-associated bloodstream infections in US intensive care units, 1997-2007. JAMA 2009; 301: 727-736.
43. Sutter DE, Milburn E, Chukwuma U, Dzialowy N, Maranich AM, Hospenthal DR. Changing susceptibility of Staphylococcus aureus in a US pediatric population. Pediatrics 2016; 137(4):e20153099.
44. Kaplan SL. Staphylococcus aureus infections in children: The implications of changing trends. Pediatrics 2016; 137(4): e20160101.
45. Wisplinghoff H, Rosato AE, Enright MC, Noto M, Craig W, Archer GL. Related clones containing SCCmec Type IV predominate among clinically significant Staphylococcus epidermidis isolates. Antimicrob Agents Chemother 2003; 47: 3574-3579.
46. Hiramatsu K, Cui L, Kuroda M, Ito T. The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 2001; 9: 486-493.
47. Iravani Mohammad Abadi M, Moniri R, Khorshidi A, Piroozmand A, Mousavi SGA, Dastehgoli K, et al. Molecular characteristics of nasal carriage methicillin-resistant coagulase negative staphylococci in school students. Jundishapur J Microbiol 2015; 8(6): e18591.
48. Miragaia M, Couto I, De Lencastre H. Genetic diversity among methicillin-resistant Staphylococcus epidermidis (MRSE). Microb Drug Resist 2005; 11: 83-93.
49. Ibrahem S, Salmenlinna S, Virolainen A, Kerttula A-M, Lyytikainen O, Jägerroos H, et al. Carriage of methicillin-resistant staphylococci and their SCCmec types in a long-term-care facility. J Clin Microbiol 2009; 47: 32-37.
50. Streit JM, Jones RN, Sader HS, Fritsche TR. Assessment of pathogen occurrences and resistance profiles among infected patients in the intensive care unit: Report from the SENTRY Antimicrobial Surveillance Program (North America, 2001). Int J Antimicrob Agents 2004; 24: 111-118.
51. Weinstein RA. Controlling antimicrobial resistance in hospitals: Infection control and use of antibiotics. Emerg Infect Dis 2001; 7: 188-192.
52. Piette A, Verschraegen G. Role of coagulase-negative staphylococci in human disease. Vet Microbiol 2009; 134: 45-54.
53. Anvari MS, Kianinejad R, Ali Boroumand M, Arzhan S, Jalali A. Bacterial pericarditis and antimicrobial resistance at the Tehran heart center, Iran. J Infect Dev Ctries 2015; 9: 780-784.
| Files | ||
| Issue | Vol 15 No 1 (2023) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i1.11913 | |
| Keywords | ||
| Iran; Meta-analysis; Methicillin resistant; Staphylococcus epidermidis; Systematic review | ||
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How to Cite
1.
Soroush S, Rezaei F, Ghanbari F, Halimi S, Taherikalani M. A five-year systematic review and meta-analysis study on methicillin resistant Staphylococcus epidermidis strains in Iran. Iran J Microbiol. 2023;15(1):10-18.
