Molecular epidemiology of antimicrobial resistant microorganisms in the 21th century: a review of the literature MDR molecular epidemiology in the 21th century

Main Article Content

Cristina Genovese
Vincenza La Fauci
Smeralda D'Amato
Andrea Squeri
Carmelina Anzalone
Gaetano Bruno Costa
Francesco Fedele
Raffaele Squeri

Keywords

Molecular, epidemiology, healthcare, associated, infections

Abstract

Healthcare-associated infections (HAIs) are the most frequent and severe complication acquired in healthcare settings with high impact in terms of morbidity, mortality and costs. Many bacteria could be implicated in these infections, but, expecially multidrug resistance bacteria could play an important role. Many microbial typing technologies have been developed until to the the bacterial whole-genome sequencing and the choice of a molecular typing method therefore will depend on the skill level and resources of the laboratory and the aim and scale of the investigation. In several studies the molecular investigation of pathogens involved in HAIs was performed with many microorganisms identified as causative agents such as Pseudomonas aeruginosa, Escherichia coli, Klebsiella pneumoniae, Clostridium difficile, Acinetobacter spp., Enterobacter spp., Enterococcus spp., Staphylococcus aureus and several more minor species. Here, we will describe the most and least frequently reported clonal complex, sequence types and ribotypes with their worldwide geographic distribution for the most important species involved in HAIs.

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References

1. Magiorakos AP, Srinivasan A, Carey RB et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18(3): 268-81. doi: 10.1111/j.1469-0691.2011.03570. x.
2. Mirande C, Bizine I, Giannetti A, Picot N, van Belkum A. Epidemiological aspects of healthcare-associated infections and microbial genomics. Eur J Clin Microbiol Infect Dis 2018; 37(5): 823-31. doi: 10.1007/s10096-017-3170-x.
3. Ehrlich GD, Post JC. The Time Is Now for Gene- and Genome-Based Bacterial Diagnostics: “You Say You Want a Revolution”. JAMA 2013; 173(15): 1405-6. doi: 10.1001/jamainternmed. 2013.7042.
4. Franco-Duarte R, Černáková L, Kadam S, et al. Advances in Chemical and Biological Methods to Identify Microorganisms-From Past to Present. Microorganisms 2019; 7(5). pii: E130. doi: 10.3390/microorganisms7050130. Review.
5. Quainoo S, Coolen JPM, van Hijum SAFT, et al. Whole-Genome Sequencing of Bacterial Pathogens: The Future of Nosocomial Outbreak Analysis. Clin Microbiol Rev 2017; 30(4): 1015-63. doi: 10.1128/CMR.00016-17. Review. Erratum in: Clin Microbiol Rev. 2017 Nov 1; 31(1).
6. Ranjbar R, Karami A, Farshad S, Giammanco GM, Mammina C. Typing methods used in the molecular epidemiology of microbial pathogens: a how-to guide. New Microbiol 2014; 37(1): 1-15. Epub 2014 Jan 15. Review.
7. Signorelli C. Molecular epidemiology in healthcare-associated infections: guidelines of the Italian Society of Hygiene, Preventive Medicine and Public Health (SItI). Ig Sanita Pubbl 2015; 71(3): 241-3.
8. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 2009; 62(10): e1-34. doi: 10.1016/j.jclinepi.2009.06. 006 PMID: 19631507.
9. Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. Available on: www.cochrane-handbook.org
10. Huang CC, Ho CM, Chen HC, et al. Evaluation of double locus (clfB and spa) sequence typing for studying molecular epidemiology of methicillin-resistantStaphylococcus aureus in Taiwan. J Microbiol Immunol Infect 2017; 50(5): 604-12. doi: 10.1016/j.jmii.2015.10.002.
11. Chen YJ, Liu KL, Chen CJ, Huang YC. Comparative Molecular Characteristics of Community-Associated and Healthcare-Associated Methicillin-Resistant Staphylococcus aureus Isolates From Adult Patients in Northern Taiwan. Medicine (Baltimore) 2015; 94(49): e1961. doi: 10.1097/MD.0000000000001961.
12. Wu D, Wang Z, Wang H, et al. Predominance of ST5-II-t311 clone among healthcare-associated methicillin-resistant Staphylococcus aureus isolates recovered from Zhejiang, China. Int J Infect Dis 2018; 71: 107-12. doi: 10.1016/j.ijid.2018.04.798.
13. Cho OH, Park KH, Song JY, et al. Prevalence and Microbiological Characteristics of qacA/B-Positive Methicillin-Resistant Staphylococcus aureus Isolates in a Surgical Intensive Care Unit. Microb Drug Resist 2018; 24(3): 283-9. doi: 10.1089/mdr.2017.0072.
14. Sonnevend Á, Blair I, Alkaabi M, et al. Change in meticillin-resistant Staphylococcus aureus clones at a tertiary care hospital in the United Arab Emirates over a 5-year period. J Clin Pathol 2012; 65(2): 178-82. doi: 10.1136/jclinpath-2011-200436.
15. Nakaminami H, Noguchi N, Ito A, et al. Characterization of methicillin-resistant Staphylococcus aureus isolated from tertiary care hospitals in Tokyo, Japan. J Infect Chemother 2014; 20(8): 512-5. doi: 10.1016/j.jiac.2014.03.006.
16. Chen X, Wang WK, Han LZ, et al. Epidemiological and genetic diversity of Staphylococcus aureus causing bloodstream infection in Shanghai, 2009-2011. PLoS One 2013; 8(9): e72811. doi: 10.1371/journal.pone.0072811.
17. Gu FF, Han LZ, Chen X, et al. Molecular characterization of Staphylococcus aureus from surgical site infections in orthopedic patients in an orthopedic trauma clinical medical center in Shanghai. Surg Infect (Larchmt) 2015; 16(1): 97-104. doi: 10.1089/sur.2014.027.
18. Wu HS, Kuo SC, Chen LY, et al. Comparison between patients under hemodialysis with community-onset bacteremia caused by community-associated and healthcare-associated methicillin-resistant Staphylococcus aureus strains. J Microbiol Immunol Infect 2013; 46(2): 96-103. doi: 10.1016/j.jmii.2012.02.004. Epub 2012 Apr 19.
19. Huang YC, Ho CF, Chen CJ, Su LH, Lin TY. Comparative molecular analysis of community-associated and healthcare-associated methicillin-resistant Staphylococcus aureus isolates from children in northern Taiwan. Clin Microbiol Infect 2008; 14(12): 1167-72. doi: 10.1111/j.1469-0691.2008.02115.x.
20. Wu TH, Lee CY, Yang HJ, et al. Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus among nasal carriage strains isolated from emergency department patients and healthcare workers in central Taiwan. J Microbiol Immunol Infect 2019; 52(2): 248-54. doi: 10.1016/j.jmii.2018.08.15.
21. Kang S, Lee J, Kim M. Medicine The association between Staphylococcus aureus nasal colonization and symptomatic infection in children in Korea where ST72 is the major genotype: A prospective observational study. Medicine (Baltimore) 2017; 96(34): e7838. doi: 10.1097/MD.0000000000007838.
22. Singh A, Prasad KN, Rahman M, et al. High frequency of SCCmec type V and agr type I among heterogeneous vancomycin-intermediate Staphylococcus aureus (hVISA) in north India. J Glob Antimicrob Resist 2017; 8: 110-14. doi: 10.1016/j.jgar.2016.11.006.
23. Wu HS, Kuo SC, Chen LY, et al. Comparison between patients under hemodialysis with community-onset bacteremia caused by community-associated and healthcare-associated methicillin-resistant Staphylococcus aureus strains. J Microbiol Immunol Infect 2013; 46(2): 96-103. doi: 10.1016/j.jmii.2012.02.004.
24. Chen YJ, Chen PA, Chen CJ, Huang YC. Molecular characteristics and clinical features of pediatric methicillin-susceptible Staphylococcus aureus infection in a medical center in northern Taiwan. BMC Infect Dis 2019; 19(1): 402. doi: 10.1186/s12879-019-4033-0.
25. Chen PY, Chuang YC, Wang JT, Chang SC. Impact of prior healthcare-associated exposure on clinical and molecular characterization of methicillin-susceptible Staphylococcus aureus bacteremia: results from a retrospective cohort study. Medicine (Baltimore). 2015; 94(5): e474. doi: 10.1097/MD.0000000000000474.
26. Jain S, Chowdhury R, Datta M, Chowdhury G, Mukhopadhyay AK. Characterization of the clonal profile of methicillin resistant Staphylococcus aureus isolated from patients with early post-operative orthopedic implant-based infections. Ann Clin Microbiol Antimicrob 2019; 18(1): 8. doi: 10.1186/s12941-019-0307-z.
27. Uehara Y, Mori M, Tauchi M, et al. First report on USA300 outbreak in a neonatal intensive care unit detected by polymerase chain reaction-based open reading frame typing in Japan. J Infect Chemother 2019; 25(5): 400-3. doi: 10.1016/j.jiac.2018.12.002. Epub 2018 Dec 28.
28. Hon PY, Koh TH, Tan TY, et al. Changing molecular epidemiology and high rates of mupirocin resistance among meticillin-resistant Staphylococcus aureus in Singaporean hospitals. J Glob Antimicrob Resist. 2014 Mar;2(1):53-55. doi: 10.1016/j.jgar.2013.10.002.
29. Hetem DJ, Derde LP, Empel J, et al. Molecular epidemiology of MRSA in 13 ICUs from eight European countries. J Antimicrob Chemother 2016; 71(1): 45-52. doi: 10.1093/jac/dkv298.
30. Mkrtchyan HV, Xu Z, Yacoub M, et al. Detection of diverse genotypes of Methicillin-resistant Staphylococcus aureus from hospital personnel and the environment in Armenia. Antimicrob Resist Infect Control 2017; 6: 19. doi: 10.1186/s13756-017-0169-0.
31. Mammina C, Calà C, Bonura C, et al. Polyclonal non multiresistant methicillin resistant Staphylococcus aureus isolates from clinical cases of infection occurring in Palermo, Italy, during a one-year surveillance period. Ann Clin Microbiol Antimicrob 2012; 11: 17. doi: 10.1186/1476-0711-11-17.
32. Espadinha D, Faria NA, Miragaia M, et al. Extensive dissemination of methicillin-resistant Staphylococcus aureus (MRSA) between the hospital and the community in a country with a high prevalence of nosocomial MRSA. PLoS One 2013; 8(4): e59960. doi: 10.1371/journal.pone.0059960.
33. Hetem DJ, Westh H, Boye K, Jarløv JO, Bonten MJ, Bootsma MC. Nosocomial transmission of community-associated methicillin-resistant Staphylococcus aureus in Danish Hospitals. J Antimicrob Chemother 2012; 67(7): 1775-80. doi: 10.1093/jac/dks125.
34. Rodríguez-Baño J, Angeles Domínguez M, Blas Millán A, et al. Clinical and molecular epidemiology of community-acquired, healthcare-associated and nosocomial methicillin-resistant Staphylococus aureus in Spain. Clin Microbiol Infect 2009; 15(12): 1111-8. doi: 10.1111/j.1469-0691.2009.02717.x.
35. González-Domínguez M, Seral C, Potel C, et al. Antimicrobial resistance, virulence factors and genetic lineages of hospital-onset methicillin-resistant Staphylococcus aureus isolates detected in a hospital in Zaragoza. Enferm Infecc Microbiol Clin 2015; 33(9): 590-6. doi: 10.1016/j.eimc.2015.01.015.
36. Szymanek-Majchrzak K, Mlynarczyk A, Mlynarczyk G Characteristics of glycopeptide-resistant Staphylococcus aureus strains isolated from inpatients of three teaching hospitals in Warsaw, Poland. Antimicrob Resist Infect Control 2018; 7: 105. doi: 10.1186/s13756-018-0397-y.
37. Reich PJ, Boyle MG, Hogan PG, et al. Emergence of community-associated methicillin-resistant Staphylococcus aureus strains in the neonatal intensive care unit: an infection prevention and patient safety challenge. Clin Microbiol Infect 2016; 22(7): 645.e1-8. doi: 10.1016/j.cmi.2016.04.013.
38. Drougka E, Foka A, Liakopoulos A, et al. A 12-year survey of methicillin-resistant Staphylococcus aureus infections in Greece: ST80-IV epidemic? Clin Microbiol Infect 2014; 20(11): O796-803. doi: 10.1111/1469-0691.12624.
39. Vandendriessche S, Hallin M, Catry B, et al. Previous healthcare exposure is the main antecedent for methicillin-resistant Staphylococcus aureus carriage on hospital admission in Belgium. Eur J Clin Microbiol Infect Dis 2012; 31(9): 2283-92. doi: 10.1007/s10096-012-1567-0.
40. Ellington MJ, Yearwood L, Ganner M, East C, Kearns AM. Distribution of the ACME-arcA gene among methicillin-resistant Staphylococcus aureus from England and Wales. J Antimicrob Chemother 2008; 61(1): 73-7.
41. Ugolotti E, Di Marco E, Bandettini R, Biassoni R. Genomic characterization of a paediatric MRSA outbreak by next-generation sequencing. J Hosp Infect 2018; 98(2): 155-60. doi: 10.1016/j.jhin.2017.08.009.
42. Velasco C, López-Cortés LE, Caballero FJ, et al. Clinical and molecular epidemiology of meticillin-resistant Staphylococcus aureus causing bacteraemia in Southern Spain. J Hosp Infect 2012; 81(4): 257-63. doi: 10.1016/j.jhin.2012.05.007.
43. Miller R, Walker AS, Knox K et al. 'Feral' and 'wild'-type methicillin-resistant Staphylococcus aureus in the United Kingdom. Epidemiol Infect 2010; 138(5): 655-65. doi: 10.1017/S0950268809991294.
44. Hultén KG, Kaplan SL, Lamberth LB et al. Hospital-acquired Staphylococcus aureus infections at Texas Children's Hospital, 2001-2007. Infect Control Hosp Epidemiol 2010; 31(2): 183-90. doi: 10.1086/649793.
45. Hudson LO, Murphy CR, Spratt BG et al. Diversity of methicillin-resistant Staphylococcus aureus (MRSA) strains isolated from inpatients of 30 hospitals in Orange County, California. PLoS One 2013; 8(4): e62117. doi: 10.1371/journal.pone.0062117.
46. Diekema DJ, Richter SS, Heilmann KP, et al. Continued emergence of USA300 methicillin-resistant Staphylococcus aureus in the United States: results from a nationwide surveillance study. Infect Control Hosp Epidemiol 2014; 35(3): 285-92. doi: 10.1086/675283.
47. Tattevin P, Schwartz BS, Graber CJ, et al. Concurrent epidemics of skin and soft tissue infection and bloodstream infection due to community-associated methicillin-resistant Staphylococcus aureus. Clin Infect Dis 2012; 55(6): 781-8. doi: 10.1093/cid/cis527.
48. Márquez-Ortiz RA, Álvarez-Olmos MI, Escobar Pérez JA, et al. USA300-related methicillin-resistant Staphylococcus aureus clone is the predominant cause of community and hospital MRSA infections in Colombian children. Int J Infect Dis 2014; 25: 88-93. doi: 10.1016/j.ijid.2014.01.008.
49. Jamrozy DM, Harris SR, Mohamed N, et al. Pan-genomic perspective on the evolution of the Staphylococcus aureus USA300 epidemic. Microb Genom 2016; 2(5): e000058. doi: 10.1099/mgen.0.000058.
50. Jenkins TC, McCollister BD, Sharma R, et al. Epidemiology of healthcare-associated bloodstream infection caused by USA300 strains of methicillin-resistant Staphylococcus aureus in 3 affiliated hospitals. Infect Control Hosp Epidemiol 2009; 30(3): 233-41. doi: 10.1086/595963.
51. Carrillo-Marquez MA(1), Hulten KG, Mason EO, Kaplan SL. Clinical and molecular epidemiology of Staphylococcus aureus catheter-related bacteremia in children. Pediatr Infect Dis J 2010; 29(5): 410-4. doi: 10.1097/INF.0b013e3181c767b6.
52. Bush K, Leal J, Fathima S, et al. The molecular epidemiology of incident methicillin-resistant Staphylococcus aureus cases among hospitalized patients in Alberta, Canada: a retrospective cohort study. Antimicrob Resist Infect Control 2015; 4: 35. doi: 10.1186/s13756-015-0076-1.
53. Eko KE, Forshey BM, Carrel M, Schweizer ML, Perencevich EN, Smith TC. Molecular characterization of methicillin-resistant Staphylococcus aureus (MRSA) nasal colonization and infection isolates in a Veterans Affairs hospital. Antimicrob Resist Infect Control 2015; 4: 10. doi: 10.1186/s13756-015-0048-5.
54. Frisch MB, Castillo-Ramírez S, Petit RA 3rd, et al. Invasive Methicillin-Resistant Staphylococcus aureus USA500 Strains from the U.S. Emerging Infections Program Constitute Three Geographically Distinct Lineages. mSphere. 2018; 3(3). pii: e00571-17. doi: 10.1128/mSphere.00571-17.
55. Nair N, Kourbatova E, Poole K, et al. Molecular epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) among patients admitted to adult intensive care units: the STAR*ICU trial. Infect Control Hosp Epidemiol 2011; 32(11): 1057-63. doi: 10.1086/662178.
56. Ocampo AM, Vélez LA, Robledo J, Jiménez JN. Changes over time in the distribution of dominant clonal complexes of methicillin-resistant Staphylococcus aureus in Medellín, Colombia. Biomedica. 2014; 34(Suppl 1): 34-40. doi: 10.1590/S0120-41572014000500005.
57. Medina G, Egea AL, Otth C, et al. Molecular epidemiology of hospital-onset methicillin-resistant Staphylococcus aureus infections in Southern Chile. Eur J Clin Microbiol Infect Dis 2013 Dec;32(12):1533-40. doi: 10.1007/s10096-013-1907-8.
58. Lévesque S, Bourgault AM, Galarneau LA, Moisan D, Doualla-Bell F, Tremblay C. Molecular epidemiology and antimicrobial susceptibility profiles of methicillin-resistant Staphylococcus aureus blood culture isolates: results of the Quebec Provincial Surveillance Programme. Epidemiol Infect 2015; 143(7): 1511-8. doi: 10.1017/S095026881400209X.
59. Peterson AE, Davis MF, Julian KG et al. Molecular and phenotypic characteristics of healthcare- and community-associated methicillin-resistant Staphylococcus aureus at a rural hospital. PLoS One 2012; 7(6): e38354. doi: 10.1371/journal.pone.0038354.
60. Uhlemann AC, Hafer C, Miko BA, et al. Clin Emergence of sequence type 398 as a community- and healthcare-associated methicillin-susceptible Staphylococcus aureus in northern Manhattan. Infect Dis 2013; 57(5): 700-3. doi: 10.1093/cid/cit375.
61. Williamson DA, Roberts SA, Ritchie SR, Coombs GW, Fraser JD, Heffernan H. Clinical and molecular epidemiology of methicillin-resistant Staphylococcus aureus in New Zealand: rapid emergence of sequence type 5 (ST5)-SCCmec-IV as the dominant community-associated MRSA clone. PLoS One 2013; 8(4): e62020. doi: 10.1371/journal.pone.0062020.
62. Coombs GW, Daley DA, Lee YT, Pang S. Australian Group on Antimicrobial Resistance (AGAR) Australian Staphylococcus aureus Sepsis Outcome Programme (ASSOP) Annual Report 2017. Commun Dis Intell (2018) 2019; 43. doi: 10.33321/cdi.2019.43.43.
63. Coombs GW, Pearson JC, Nimmo GR et al. Antimicrobial susceptibility of Staphylococcus aureus and molecular epidemiology of meticillin-resistant S. aureus isolated from Australian hospital inpatients: Report from the Australian Group on Antimicrobial Resistance 2011 Staphylococcus aureus Surveillance Programme. J Glob Antimicrob Resist 2013; 1(3): 149-56. doi: 10.1016/j.jgar.2013.04.005.
64. Hewagama S, Spelman T, Woolley M, McLeod J, Gordon D, Einsiedel L. The Epidemiology of Staphylococcus aureus and Panton-Valentine Leucocidin (pvl) in Central Australia, 2006-2010. BMC Infect Dis 2016; 16: 382. doi: 10.1186/s12879-016-1698-5.
65. Bouiller K, Gbaguidi-Haore H, Hocquet D, Cholley P, Bertrand X, Chirouze C. Clonal complex 398 methicillin-susceptible Staphylococcus aureus bloodstream infections are associated with high mortality. Clin Microbiol Infect 2016; 22(5): 451-5. doi: 10.1016/j.cmi.2016.01.018.
66. Egyir B, Oteng AA, Owusu E, Newman MJ, Addo KK, Rhod Larsen A. Characterization of Staphylococcus aureus from human immunodeficiency virus (HIV) patients in Accra, Ghana. J Infect Dev Ctries 2016;10: 453-6.
67. BenDarif E, Khalil A, Rayes A, et al.Characterization of methicillin-resistant Staphylococcus aureus isolated at Tripoli Medical Center, Libya, between 2008 and 2014. J Med Microbiol 2016; 65(12): 1472-5. doi: 10.1099/jmm.0.000384. Epub 2016 Nov 1.
68. Perovic O, Singh-Moodley A, Govender NP, et al. A small proportion of community-associated methicillin-resistant Staphylococcus aureus bacteraemia, compared to healthcare-associated cases, in two South African provinces. Eur J Clin Microbiol Infect Dis 2017; 36(12): 2519-32. doi: 10.1007/s10096-017-3096-3.
69. Conceição T, Coelho C, de Lencastre H, Aires-de-Sousa M. Frequent occurrence of oxacillin-susceptible mecA-positive Staphylococcus aureus (OS-MRSA) strains in two African countries. J Antimicrob Chemother 2015; 70(12): 3200-4. doi: 10.1093/jac/dkv261.
70. Boswihi SS, Udo EE, Al-Sweih N. Shifts in the Clonal Distribution of Methicillin-Resistant Staphylococcus aureus in Kuwait Hospitals: 1992-2010. PLoS One 2016; 11(9): e0162744. doi: 10.1371/journal.pone.0162744.
71. Omuse G, Van Zyl KN, Hoek K Molecular characterization of Staphylococcus aureus isolates from various healthcare institutions in Nairobi, Kenya: a cross sectional study. Ann Clin Microbiol Antimicrob 2016; 15(1): 51. doi: 10.1186/s12941-016-0171-z.
72. Alioua MA, Labid A, Amoura K, Bertine M, Gacemi-Kirane D, Dekhil M. Emergence of the European ST80 clone of community-associated methicillin-resistant Staphylococcus aureus as a cause of healthcare-associated infections in Eastern Algeria. Med Mal Infect 2014; 44(4): 180-3. doi: 10.1016/j.medmal.2014.01.006.
73. Udo EE, Sarkhoo E. The dissemination of ST80-SCCmec-IV community-associated methicillin resistant Staphylococcus aureus clone in Kuwait hospitals. Ann Clin Microbiol Antimicrob 2010; 9: 31. doi: 10.1186/1476-0711-9-31.
74. Conceição T, Coelho C, Santos-Silva I, de Lencastre H, Aires-de-Sousa M. Epidemiology of methicillin-resistant and -susceptible Staphylococcus aureus in Luanda, Angola: first description of the spread of the MRSA ST5-IVa clone in the African continent. Microb Drug Resist 2014; 20(5): 441-9. doi: 10.1089/mdr.2014.0007.
75. El-Mahdy TS, El-Ahmady M, Goering RV. Molecular characterization of methicillin-resistant Staphylococcus aureus isolated over a 2-year period in a Qatari hospital from multinational patients. Clin Microbiol Infect 2014; 20(2): 169-73. doi: 10.1111/1469-0691.12240.
76. Miragaia M, Carriço JA, Thomas JC, Couto I, Enright MC, de Lencastre H. Comparison of molecular typing methods for characterization of Staphylococcus epidermidis: proposal for clone definition. J Clin Microbiol 2008; 46(1): 118-29.
77. Willemse-Erix HF, Jachtenberg J, Barutçi H, et al. Proof of principle for successful characterization of methicillin-resistant coagulasenegative staphylococci isolated from skin by use of Raman spectroscopy and pulsed-field gel electrophoresis. J Clin Microbiol 2010; 48(3): 736-40.
78. 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(7): 570-577.
79. Du X, Zhu Y, Song Y, et al. Molecular analysis of Staphylococcus epidermidis strains isolated from community and hospital environments in China. PLoS One 2013; 8(5): e62742. doi: 10.1371/journal.pone.0062742. Print 2013.
80. Corredor NC, López C, Aguilera PA, et al. An epidemiological and molecular study regarding the spread of vancomycin-resistant Enterococcus faecium in a teaching hospital in Bogotá, Colombia 2016. BMC Infect Dis 2019; 19(1): 258. doi: 10.1186/s12879-019-3.
81. Raven KE, Reuter S, Reynolds R, et al. A decade of genomic history for healthcare-associated Enterococcus faecium in the United Kingdom and Ireland. Genome Res 2016; 26(10): 1388-96.
82. Sundermann AJ, Babiker A, Marsh JW, et al. Outbreak of Vancomycin-resistant Enterococcus faecium in Interventional Radiology: Detection Through Whole Genome Sequencing-Based Surveillance. Clin Infect Dis 2019;. pii: ciz666. doi: 10.1093/cid/ciz666.
83. Abbo L, Shukla BS, Giles A, et al. Linezolid- and Vancomycin-resistant Enterococcus faecium in Solid Organ Transplant Recipients: Infection Control and Antimicrobial Stewardship Using Whole Genome Sequencing. Clin Infect Dis 2019; 69(2): 259-65. doi: 10.1093/cid/ciy903.
84. Leal HF, Azevedo J, Silva GEO, et al. Bloodstream infections caused by multidrug-resistant gram-negative bacteria: epidemiological, clinical and microbiological features. BMC Infect Dis 2019; 19(1): 609. doi: 10.1186/s12879-019-4265-z.
85. Can F, Kurt-Azap Ö, İspir P, et al. The clinical impact of ST131 H30-Rx subclone in urinary tract infections due to multidrug-resistant Escherichia coli. J Glob Antimicrob Resist 2016; 4: 49-52. doi: 10.1016/j.jgar.2015.10.006.
86. Merino I, Shaw E, Horcajada JP, et al. CTX-M-15-H30Rx-ST131 subclone is one of the main causes of healthcare-associated ESBL-producing Escherichia coli bacteraemia of urinary origin in Spain. J Antimicrob Chemother 2016; 71(8): 2125-30. doi: 10.1093/jac/dkw133.
87. Ciesielczuk H, Jenkins C, Chattaway M, et al. Trends in ExPEC serogroups in the UK and their significance. Eur J Clin Microbiol Infect Dis 2016; 35(10): 1661-6. doi: 10.1007/s10096-016-2707-8.
88. Burke L, Humphreys H, Fitzgerald-Hughes D. The Molecular Epidemiology of Resistance in Cefotaximase-Producing Escherichia coli Clinical Isolates from Dublin, Ireland. Microb Drug Resist 2016; 22(7): 552-8. Epub 2016 Mar 22.
89. Riley LW. Pandemic lineages of extraintestinal pathogenic Escherichia coli. Clin Microbiol Infect 2014; 20(5): 380-90. doi: 10.1111/1469-0691.12646.
90. Samuelsen Ø, Overballe-Petersen S, Bjørnholt JV, et al. Molecular and epidemiological characterization of carbapenemase-producing Enterobacteriaceae in Norway, 2007 to 2014. PLoS One 2017; 12(11): e0187832. doi: 10.1371/journal.pone.0187832.
91. Pitout JD. Infections with extended-spectrum beta-lactamase-producing enterobacteriaceae: changing epidemiology and drug treatment choices. Drugs 2010; 70(3): 313-33. doi: 10.2165/11533040-000000000-00000.
92. Kim YA, Kim JJ, Kim H, Lee K. Community-onset extended-spectrum-β-lactamase-producing Escherichia coli sequence type 131 at two Korean community hospitals: The spread of multidrug-resistant E. coli to the community via healthcare facilities. Int J Infect Dis 2017; 54: 39-42. doi: 10.1016/j.ijid.2016.11.010.
93. Croxall G, Hale J, Weston V, et al. Molecular epidemiology of extraintestinal pathogenic Escherichia coli isolates from a regional cohort of elderly patients highlights the prevalence of ST131 strains with increased antimicrobial resistance in both community and hospital care settings. J Antimicrob Chemother 2011; 66(11): 2501-8. doi: 10.1093/jac/dkr349. Epub 2011 Aug 22.
94. Kim H, Kim YA, Park YS, Choi MH, Lee GI, Lee K. Risk Factors and Molecular Features of Sequence Type (ST) 131 Extended-spectrum β-Lactamase-producing Escherichia coli in Community-onset Bacteremia. Sci Rep 2017; 7(1): 14640. doi: 10.1038/s41598-017-14621-4.
95. Weissman SJ, Hansen NI, Zaterka-Baxter K, Higgins RD, Stoll BJ. Emergence of Antibiotic Resistance-Associated Clones Among Escherichia coli Recovered From Newborns With Early-Onset Sepsis and Meningitis in the United States, 2008-2009. J Pediatric Infect Dis Soc 2016; 5(3): 269-76. doi: 10.1093/jpids/piv013.
96. Suzuki S, Shibata N, Yamane K, Wachino J, Ito K, Arakawa Y. Change in the prevalence of extended-spectrum-beta-lactamase-producing Escherichia coli in Japan by clonal spread. J Antimicrob Chemother 2009; 63(1): 72-9. doi: 10.1093/jac/dkn463.
97. Salipante SJ, Roach DJ, Kitzman JO, et al. Large-scale genomic sequencing of extraintestinal pathogenic Escherichia coli strains. Genome Res 2015; 25(1): 119-28. doi: 10.1101/gr.180190.114.
98. Grundmann H, Glasner C, Albiger B, et al. Occurrence of carbapenemase-producing Klebsiella pneumoniae and Escherichia coli in the European survey of carbapenemase-producing Enterobacteriaceae (EuSCAPE): a prospective, multinational study. Lancet Infect Dis 2017; 17(2): 153-63. doi: 10.1016/S1473-3099(16)30257-2.
99. Roer L, Overballe-Petersen S, Hansen F, et al. Escherichia coli Sequence Type 410 Is Causing New International High-Risk Clones. mSphere. 2018;3(4). pii: e00337-18. doi: 10.1128/mSphere.00337-18.
100. Clancy CJ, Chen L, Shields RK, et al. Epidemiology and molecular characterization of bacteremia due to carbapenem-resistant Klebsiella pneumoniae in transplant recipients. Am J Transplant 2013; 13(10): 2619-33. doi: 10.1111/ajt.12424.
101. Endimiani A, Depasquale JM, Forero S, et al. Emergence of blaKPC-containing Klebsiella pneumoniae in a long-term acute care hospital: a new challenge to our healthcare system. J Antimicrob Chemother 2009; 64(5): 1102-10. doi: 10.1093/jac/dkp327.
102. Rojas LJ, Weinstock GM, De La Cadena E, et al. An Analysis of the Epidemic of Klebsiella pneumoniae Carbapenemase-Producing K. pneumoniae: Convergence of Two Evolutionary Mechanisms Creates the "Perfect Storm". J Infect Dis 2017; 217(1): 82-92. doi: 10.1093/infdis/jix524.
103. Zautner AE, Bunk B, Pfeifer Y, et al. Monitoring microevolution of OXA-48-producing Klebsiella pneumoniae ST147 in a hospital setting by SMRT sequencing. Antimicrob Chemother 2017; 72(10): 2737-2744. doi: 10.1093/jac/dkx216.
104. Bowers JR, Kitchel B, Driebe EM et, al. Genomic Analysis of the Emergence and Rapid Global Dissemination of the Clonal Group 258 Klebsiella pneumoniae Pandemic. PLoS One 2015; 10(7): e0133727. doi: 10.1371/journal.pone.0133727.
105. Capone A, Giannella M, Fortini D, et al. High rate of colistin resistance among patients with carbapenem-resistant Klebsiella pneumoniae infection accounts for an excess of mortality. Clin Microbiol Infect 2013; 19(1): E23-E30. doi: 10.1111/1469-0691.12070.
106. Palacios-Baena ZR, Oteo J, Conejo C, et al. Comprehensive clinical and epidemiological assessment of colonisation and infection due to carbapenemase-producing Enterobacteriaceae in Spain. J Infect 2016; 72(2): 152-60. doi: 10.1016/j.jinf.2015.10.008.
107. Kim JO, Song SA, Yoon EJ, et al. Outbreak of KPC-2-producing Enterobacteriaceae caused by clonal dissemination of Klebsiella pneumoniae ST307 carrying an IncX3-type plasmid harboring a truncated Tn4401a. Diagn Microbiol Infect Dis 2017; 87(4): 343-8. doi: 10.1016/j.diagmicrobio.2016.12.012.
108. Aqel AA, Giakkoupi P, Alzoubi H, Masalha I, Ellington MJ, Vatopoulos A. Detection of OXA-48-like and NDM carbapenemases producing Klebsiella pneumoniae in Jordan: A pilot study. J Infect Public Health 2017; 10(2): 150-5. doi: 10.1016/j.jiph.2016.02.002.
109. Clarivet B, Grau D, Jumas-Bilak E, et al. Persisting transmission of carbapenemase-producing Klebsiella pneumoniae due to an environmental reservoir in a university hospital, France, 2012 to 2014. Euro Surveill 2016; 21(17). doi: 10.2807/1560-7917.ES.2016.21.17.30213.
110. Cubero M, Grau I, Tubau F, et al. Molecular Epidemiology of Klebsiella pneumoniae Strains Causing Bloodstream Infections in Adults. Microb Drug Resist 2018; 24(7): 949-57. doi: 10.1089/mdr.2017.0107.
111. Fursova NK, Astashkin EI, Knyazeva AI, et al. The spread of bla OXA-48 and bla OXA-244 carbapenemase genes among Klebsiella pneumoniae, Proteus mirabilis and Enterobacter spp. isolated in Moscow, Russia. Ann Clin Microbiol Antimicrob 2015; 14: 46. doi: 10.1186/s12941-015-0108-y.
112. Vanegas JM, Parra OL, Jiménez JN. Molecular epidemiology of carbapenem resistant gram-negative bacilli from infected pediatric population in tertiary care hospitals in Medellín, Colombia: an increasing problem. BMC Infect Dis 2016; 16: 463. doi: 10.1186/s12879-016-1805-7.
113. Apisarnthanarak A, Kiratisin P, Mundy LM. Clinical and molecular epidemiology of healthcare-associated infections due to extended-spectrum beta-lactamase (ESBL)-producing strains of Escherichia coli and Klebsiella pneumoniae that harbor multiple ESBL genes. Infect Control Hosp Epidemiol 2008; 29(11): 1026-34. doi: 10.1086/591864.
114. Abdul Momin MHF, Liakopoulos A, Phee LM, Wareham DW. Emergence and nosocomial spread of carbapenem-resistant OXA-232-producing Klebsiella pneumoniae in Brunei Darussalam. J Glob Antimicrob Resist 2017; 9: 96-9. doi: 10.1016/j.jgar.2017.02.008.
115. O'Connor C, Cormican M, Boo TW, et al. An Irish outbreak of New Delhi metallo-β-lactamase (NDM)-1 carbapenemase-producing Enterobacteriaceae: increasing but unrecognized prevalence. J Hosp Infect 2016; 94(4): 351-7. doi: 10.1016/j.jhin.2016.08.005.
116. Villa L, Feudi C, Fortini D, et al.Diversity, virulence, and antimicrobial resistance of the KPC-producing Klebsiella pneumoniae ST307 clone. Microb Genom 2017; 3(4): e000110. doi: 10.1099/mgen.0.000110.
117. Espenhain L, Jørgensen SB, Leegaard TM, et al. Travel to Asia is a strong predictor for carriage of cephalosporin resistant E. coli and Klebsiella spp. but does not explain everything; prevalence study at a Norwegian hospital 2014-2016. Antimicrob Resist Infect Control 2018; 7: 146. doi: 10.1186/s13756-018-0429-7.
118. Shankar C, Veeraraghavan B, Nabarro LEB, Ravi R, Ragupathi NKD, Rupali P. Whole genome analysis of hypervirulent Klebsiella pneumoniae isolates from community and hospital acquired bloodstream infection. BMC Microbiol 2018; 18(1): 6. doi: 10.1186/s12866-017-1148-6.
119. Meunier D, Findlay J, Doumith M, et al. FRI-2 carbapenemase-producing Enterobacter cloacae complex in the UK. J Antimicrob Chemother 2017; 72(9): 2478-82. doi: 10.1093/jac/dkx173.
120. Noël A, Vastrade C, Dupont S, et al. Nosocomial outbreak of extended-spectrum β-lactamase-producing Enterobacter cloacae among cardiothoracic surgical patients: causes and consequences. J Hosp Infect 2019; 102(1): 54-60. doi: 10.1016/j.jhin.2019.01.001.
121. Madueño A, González García J, Fernández-Romero S, Oteo J, Lecuona M. Dissemination and clinical implications of multidrug-resistant Klebsiella pneumoniae isolates producing OXA-48 in a Spanish hospital. J Hosp Infect 2017; 96(2): 116-22. doi: 10.1016/j.jhin.2017.02.024.
122. Forde C, Stierman B, Ramon-Pardo P, Dos Santos T, Singh N. Carbapenem-resistant Klebsiella pneumoniae in Barbados: Driving change in practice at the national level. PLoS One 2017; 12(5): e0176779. doi: 10.1371/journal.pone.0176779.
123. Zerr DM, Weissman SJ, Zhou C, et al. The Molecular and Clinical Epidemiology of Extended-Spectrum Cephalosporin- and Carbapenem-Resistant Enterobacteriaceae at 4 US Pediatric Hospitals. J Pediatric Infect Dis Soc 2017; 6(4): 366-75. doi: 10.1093/jpids/piw076.
124. Villa J, Arana DM, Viedma E, Perez-Montarelo D, Chaves F. Characterization of mobile genetic elements carrying VIM-1 and KPC-2 carbapenemases in Citrobacter freundii isolates in Madrid. Int J Med Microbiol 2017; 307(6): 340-5. doi: 10.1016/j.ijmm.2017.07.001.
125. Parcell BJ, Oravcova K, Pinheiro M, et al. Pseudomonas aeruginosa intensive care unit outbreak: winnowing of transmissions. with molecular and genomic typing. J Hosp Infect 2018; 98(3): 282-8. doi: 10.1016/j.jhin.2017.12.005
126. Martin K, Baddal B, Mustafa N, et al. Clusters of genetically similar isolates of Pseudomonas aeruginosa from multiple hospitals in the UK. J Med Microbiol 2013; 62(Pt 7): 988-1000. doi: 10.1099/jmm.0.054841-0. Epub 2013 Apr 4.
127. Breathnach AS, Cubbon MD, Karunaharan RN, Pope CF, Planche TD. Multidrug-resistant Pseudomonas aeruginosa outbreaks in two hospitals: association with contaminated hospital waste-water systems. J Hosp Infect 2012; 82(1): 19-24. doi: 10.1016/j.jhin.2012.06.007.
128. Giani T, Arena F, Pollini S, et al. Italian nationwide survey on Pseudomonas aeruginosa from invasive infections: activity of ceftolozane/tazobactam and comparators, and molecular epidemiology of carbapenemase producers. J Antimicrob Chemother 2018; 73(3): 664-71. doi: 10.1093/jac/dkx453.
129. Tissot F, Blanc DS, Basset P, et al. New genotyping method discovers sustained nosocomial Pseudomonas aeruginosa outbreak in an intensive care burn unit. J Hosp Infect 2016; 94(1): 2-7. doi: 10.1016/j.jhin.2016.05.011.
130. Wright LL, Turton JF, Livermore DM, Hopkins KL, Woodford N. Dominance of international 'high-risk clones' among metallo-β-lactamase-producing Pseudomonas aeruginosa in the UK. J Antimicrob Chemother 2015; 70(1): 103-10. doi: 10.1093/jac/dku339.
131. Telling K, Laht M, Brauer A, et al.Multidrug resistant Pseudomonas aeruginosa in Estonian hospitals. BMC Infect Dis 2018; 18(1): 513. doi: 10.1186/s12879-018-3421-1.
132. Tuan Anh N, Nga TV, Tuan HM, et al. Molecular epidemiology and antimicrobial resistance phenotypes of Acinetobacter baumannii isolated from patients in three hospitals in southern Vietnam. J Med Microbiol 2017; 66(1): 46-53. doi: 10.1099/jmm.0.000418.
133. Karaaslan A, Soysal A, Altinkanat Gelmez G, Kepenekli Kadayifci E, Söyletir G, Bakir M. Molecular characterization and risk factors for carbapenem-resistant Gram-negative bacilli colonization in children: emergejnce of NDM-producing Acinetobacter baumannii in a newborn intensive care unit in Turkey. J Hosp Infect 2016; 92(1): 67-72. doi: 10.1016/j.jhin.2015.09.011.
134. Nawfal Dagher T, Al-Bayssari C, Chabou S, et al. Investigation of multidrug-resistant ST2 Acinetobacter baumannii isolated from Saint George hospital in Lebanon. BMC Microbiol 2019; 19(1): 29. doi: 10.1186/s12866-019-1401-2.
135. Gómez RF, Castillo A, Chávez-Vivas M. Characterization of multidrug-resistant Acinetobacter ssp. strains isolated from medical intensive care units in Cali - Colombia. ColombMed (Cali) 2017; 48(4): 183-90. doi: 10.25100/cm.v48i4.2858.
136. da Silva KE, Maciel WG, Croda J, et al. A high mortality rate associated with multidrug-resistant Acinetobacter baumannii ST79 and ST25 carrying OXA-23 in a Brazilian intensive care unit. PLoS One 2018; 13(12): e0209367. doi: 10.1371/journal.pone.0209367.
137. Chen Y, Yang Y, Liu L, et al. High prevalence and clonal dissemination of OXA-72-producing Acinetobacter baumannii in a Chinese hospital: a cross sectional study. BMC Infect Dis 2018; 18(1): 491. doi: 10.1186/s12879-018-3359-3.
138. Saffari F, Monsen T, Karmostaji A, Azimabad FB, Widerström M. Significant spread of extensively drug-resistant Acinetobacter baumannii genotypes of clonal complex 92 among intensive care unit patients in a university hospital in southern Iran. J Med Microbiol 2017; 66(11): 1656-62. doi: 10.1099/jmm.0.000619.
139. El Bannah AMS, Nawar NN, Hassan RMM, Salem STB. Molecular Epidemiology of Carbapenem-Resistant Acinetobacter baumannii in a Tertiary Care Hospital in Egypt: Clonal Spread of blaOXA-23. Microb Drug Resist 2018; 24(3): 269-77. doi: 10.1089/mdr.2017.0057.
140. Ho PL, Ho AY, Chow KH, Lai EL, Ching P, Seto WH. Epidemiology and clonality of multidrug-resistant Acinetobacter baumannii from a healthcare region in Hong Kong. J Hosp Infect 2010; 74(4): 358-64. doi: 10.1016/j.jhin.2009.10.015.
141. de Azevedo FKSF, Dutra V, Nakazato L, et al. Molecular epidemiology of multidrug-resistant Acinetobacter baumannii infection in two hospitals in Central Brazil: the role of ST730 and ST162 in clinical outcomes. J Med Microbiol 2019; 68(1): 31-40. doi: 10.1099/jmm.0.000853. Epub 2018 Dec.
142. Nhu NTK, Lan NPH, Campbell JI, et al. Emergence of carbapenem-resistant Acinetobacter baumannii as the major cause of ventilator-associated pneumonia in intensive care unit patients at an infectious disease hospital in southern Vietnam. J Med Microbiol 2014; 63(Pt 10): 1386-94. doi: 10.1099/jmm.0.076646-0.
143. Fatima R, Aziz M. The Hypervirulent Strain of Clostridium Difficile: NAP1/B1/027 - A Brief Overview. Cureus 2019; 11(1): e3977. doi: 10.7759/cureus.3977.
144. Luo Y, Cheong E, Bian Q et, al. Different molecular characteristics and antimicrobial resistance profiles of Clostridium difficile in the Asia-Pacific region. Emerg Microbes Infect 2019; 8(1): 1553-62. doi: 10.1080/22221751.2019.1682472.
145. Cartman ST, Heap JT, Kuehne SA, Cockayne A, Minton NP. The emergence of 'hypervirulence' in Clostridium difficile. Int J Med Microbiol 2010; 300(6): 387-95. doi: 10.1016/j.ijmm.2010.04.008.
146. Freeman J1, Vernon J, Pilling S, et al. The ClosER study: results from a three-year pan-European longitudinal surveillance of antibiotic resistance among prevalent Clostridium difficile ribotypes, 2011-2014. Clin Microbiol Infect 2018; 24(7): 724-31. doi: 10.1016/j.cmi.2017.10.008. Epub 2017 Oct 21.
147. Rodriguez C, Fernandez J, Van Broeck J, et al. Clostridium difficile presence in Spanish and Belgian hospitals. Microb Pathog 2016; 100: 141-8. doi: 10.1016/j.micpath.2016.09.006.
148. Del Prete R, Ronga L, Addati G, Magrone R, Miragliotta G. Prevalence of Clostridium difficile and ribotype 027 infection in patients with nosocomial diarrhoea in Southern Italy. New Microbiol 2017; 40(4): 264-8.
149. Costa CL, Mano de Carvalho CB, González RH, et al. Molecular epidemiology of Clostridium difficile infection in a Brazilian cancer hospital. Anaerobe 2017; 48: 232-6. doi: 10.1016/j.anaerobe.2017.10.001.
150. Jia H, Du P, Yang H, et al. Nosocomial transmission of Clostridium difficile ribotype 027 in a Chinese hospital, 2012-2014, traced by whole genome sequencing. BMC Genomics 2016; 17: 405. doi: 10.1186/s12864-016-2708-0.
151. Razavi B, Apisarnthanarak A, Mundy LM. Clostridium difficile: emergence of hypervirulence and fluoroquinolone resistance. Infection 2007; 35(5): 300-7.
152. Black SR, Weaver KN, Jones RC, et al. Clostridium difficile outbreak strain BI is highly endemic in Chicago area hospitals. Infect Control Hosp Epidemiol 2011; 32(9): 897-902. doi: 10.1086/661283.
153. Walker AS, Eyre DW, Wyllie DH, et al. Characterisation of Clostridium difficile hospital ward-based transmission using extensive epidemiological data and molecular typing. PLoS Med 2012; 9(2): e1001172. doi: 10.1371/journal.pmed.1001172.
154. Dingle KE, Griffiths D, Didelot X, et al. Clinical Clostridium difficile: clonality and pathogenicity locus diversity. PLoS One 2011; 6(5): e19993. doi: 10.1371/journal.pone.0019993.
155. Foster NF, Collins DA, Ditchburn SL, et al. Epidemiology of Clostridium difficile infection in two tertiary-care hospitals in Perth, Western Australia: a cross-sectional study. New Microbes New Infect 2014; 2(3): 64-71. doi: 10.1002/nmi2.43.
156. Richardson C, Kim P, Lee C, Bersenas A, Weese JS. Comparison of Clostridium difficile isolates from individuals with recurrent and single episode of infection. Anaerobe 2015; 33: 105-8. doi: 10.1016/j.anaerobe.2015.03.003.
157. Freeman J, Vernon J, Morris K, et al. Pan-European longitudinal surveillance of antibiotic resistance among prevalent Clostridium difficile ribotypes. Clin Microbiol Infect 2015; 21(3): 248.e9-248.e16. doi: 10.1016/j.cmi.2014.09.017.
158. Santos A, Isidro J, Silva C, et al. Molecular and epidemiologic study of Clostridium difficile reveals unusual heterogeneity in clinical strains circulating in different regions in Portugal. Clin Microbiol Infect 2016; 22(8): 695-700. doi: 10.1016/j.cmi.2016.04.002.
159. Zainul NH, Ma ZF, Besari A, et al. Prevalence of Clostridium difficile infection and colonization in a tertiary hospital and elderly community of North-Eastern Peninsular Malaysia. Epidemiol Infect 2017; 145(14): 3012-9. doi: 10.1017/S0950268817002011.
160. Arvand M, Ruscher C, Bettge-Weller G, Goltz M, Pfeifer Y. Prevalence and risk factors for colonization by Clostridium difficile and extended-spectrum β-lactamase-producing Enterobacteriaceae in rehabilitation clinics in Germany. J Hosp Infect 2018; 98(1): 14-20. doi: 10.1016/j.jhin.2017.07.004.
161. Sathyendran V, McAuliffe GN, Swager T, Freeman JT, Taylor SL, Roberts SA. Clostridium difficile as a cause of healthcare-associated diarrhoea among children in Auckland, New Zealand: clinical and molecular epidemiology. Eur J Clin Microbiol Infect Dis 2014; 33(10): 1741-7. doi: 10.1007/s10096-014-2139-2.
162. Novak A, Spigaglia P, Barbanti F, Goic-Barisic I, Tonkic M. First clinical and microbiological characterization of Clostridium difficile infection in a Croatian University Hospital. Anaerobe 2014; 30: 18-23. doi: 10.1016/j.anaerobe.2014.07.007.
163. Collins DA, Putsathit P, Elliott B, Riley TV. Laboratory-based surveillance of Clostridium difficile strains circulating in the Australian healthcare setting in 2012. Pathology 2017; 49(3): 309-13. doi: 10.1016/j.pathol.2016.10.013.
164. Drabek J, Nyc O, Krutova M, Stovicek J, Matejkova J, Keil R. Clinical features and characteristics of Clostridium difficile PCR-ribotype 176 infection: results from a 1-year university hospital internal ward study. Ann Clin Microbiol Antimicrob 2015; 14: 55. doi: 10.1186/s12941-015-0114-0.
165. Kuijper EJ, Coignard B, Tüll P; ESCMID Study Group for Clostridium difficile; EU Member States; European Centre for Disease Prevention and Control. Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect 2006; 12(Suppl 6) :2-18. Review.
166. Mutters NT, Heeg K, Späth I, Henny N, Günther F. Improvement of infection control management by routine molecular evaluation of pathogen clusters. Diagn Microbiol Infect Dis 2017 May;88(1):82-87. doi: 10.1016/j.diagmicrobio.2017.01.013.
167. La Fauci V, Costa GB, Arena A, et al. Trend of MDR-microorganisms isolated from the biological samples of patients with HAI and from the surfaces around that patient. New Microbiol 2018; 41: 42-6.
168. Squeri R, Genovese C, Trimarchi G, et al. Nine years of microbiological air monitoring in the operating theatres of a university hospital in Southern Italy. Ann Ig 2019; 31(2 Suppl 1): 1-12. doi: 10.7416/ai.2019.2272.
169. La Fauci V, Genovese C, Facciolà A, et al. Five-year microbiological monitoring of wards and operating theatres in southern Italy. J Prev Med Hyg 2017; 58: E166-E172.
170. Montagna MT, Mascipinto S, Pousis C, et al. Knowledge, experiences, and attitudes toward Mantoux test among medical and health professional students in Italy: a cross-sectional study. Ann Ig 2018; 30(5 Suppl 2):86- 98. doi: 10.7416/ai.2018.2253.
171. Squeri R, Genovese C, Palamara MA, Trimarchi G, La Fauci V. "Clean care is safer care": correct handwashing in the prevention of healthcare associated infections. Ann Ig 2016; 28(6): 409-15. doi: 10.7416/ai.2016.2123.
172. La Fauci V, Costa GB, Genovese C, Palamara MAR, Alessi V, Squeri R. Drug-resistant bacteria on hands of healthcare workers and in the patient area: an environmental survey in Southern Italy's hospital. Rev Esp Quimioter 2019 Jun 28. pii: fauci28jun2019.
173. Squeri R, Grillo OC, La Fauci V. Surveillance and evidence of contamination in hospital environment from meticillin and vancomycin-resistant microbial agents. J Prev Med Hyg 2012; 53(3): 143-5.
174. La Fauci V, Riso R, Facciolà A, Merlina V, Squeri R. Surveillance of microbiological contamination and correct use of protective lead garments. Ann Ig 2016; 28(5): 360-6. doi: 10.7416/ai.2016.2116.
175. La Fauci V, Costa GB, Facciolà A, Conti A, Riso R, Squeri R.Humidifiers for oxygen therapy: what risk for reusable and disposable devices? J Prev Med Hyg. 2017 Jun;58(2):E161-E165.
176. Spagnolo EV, Cannavò G, Mondello C, Cardia L, Bartoloni G, Cardia G. Unexpected death for Takayasu aortitis associated with coronary ostial stenosis: case report. Am J Forensic Med Pathol 2015; 36(2): 88-90. doi: 10.1097/PAF.0000000000000154.
177. Rini MS, Argo A, Spagnolo EV, Zerbo S, Bucci MB, D'Urso D. When is necessary not to apply guidelines? Pitfalls in dentistry practice. Dental Cadmos 2018; 86(8): 686-95. http://www.odontoiatria33.it/ doi: 10.19256/d.cadmos.08.2018.07.
178. Ventura Spagnolo E, Mondello C, Roccuzzo S, et al. A unique fatal case of Waterhouse-Friderichsen syndrome caused by Proteus mirabilis in an immunocompetent subject: Case report and literature analysis. Medicine (Baltimore) 2019; 98(34): e16664. doi: 10.1097/MD.0000000000016664.
179. Ventura Spagnolo E, Stassi C, Mondello C, Zerbo S, Milone L, Argo A. Forensic microbiology applications: A systematic review. Leg Med (Tokyo) 2019; 36: 73-80. doi: 10.1016/j.legalmed.2018.11.002.
180. Genovese C, LA Fauci V, Squeri A, Trimarchi G, Squeri R. HPV vaccine and autoimmune diseases: systematic review and meta-analysis of the literature. J Prev Med Hyg 2018; 59(3): E194-E199. doi: 10.15167/2421-4248/jpmh2018.59.3.998.
181. Genovese C, Picerno IAM, Trimarchi G, et al. Vaccination coverage in healthcare workers: a multicenter cross-sectional study in Italy. J Prev Med Hyg 2019; 60(1): E12-E17. doi: 10.15167/2421-4248/jpmh2019.60.1.1097.
182. Squeri R, Genovese C, Trimarchi G, Palamara MAR, La Fauci V. An evaluation of attitude toward vaccines among healthcare workers of a University Hospital in Southern Italy. Ann Ig 2017; 29(6): 595-606. doi: 10.7416/ai.2017.2188.
183. La Fauci V, Sindoni D, Grillo OC, Calimeri S, Lo Giudice D, Squeri R. Hepatitis E virus (HEV) in sewage from treatment plants of Messina University Hospital and of Messina City Council. J Prev Med Hyg 2010; 51(1): 28-30.
184. Genovese C, La Fauci V, Costa GB, et al. A potential outbreak of Measles and chickenpox among healthcare workers of a university Hospital EMBJ 2019; 14(10): 045-8.
185. Squeri R, Genovese C, Trimarchi G, Palamara MAR, La Fauci V. An evaluation of attitude toward vaccines among healthcare workers of a University Hospital in Southern Italy. Ann Ig 2017; 29(6): 595-606. doi: 10.7416/ai.2017.2188.
186. Squeri R, La Fauci V, Sindoni L, Cannavò G, Ventura Spagnolo E.Study on hepatitis B and C serologic status among municipal solid waste workers in Messina (Italy). J Prev Med Hyg. 2006 Sep;47(3):110-3.
187. Ferrera G, Squeri R, Genovese C. The evolution of vaccines for early childhood: the MMRV. Ann Ig 2018; 30(4 Suppl 1): 33-7. doi: 10.7416/ai.2018.2232.
188. Lo Giudice D, Capua A, La Fauci V, Squeri R, Grillo OC, Calimeri S.Congenital rubella syndrome and immunity status of immigrant women living in southern Italy: a cross-sectional, seroepidemiological investigation. Travel Med Infect Dis. 2014 May-Jun;12(3):253-7. doi: 10.1016/j.tmaid.2014.01.003.
189. La Fauci V, Riso R, Facciolà A, et al. Response to anti-HBV vaccine and 10-year follow-up of antibody levels in healthcare workers. Public Health 2016; 139: 198-202. doi: 10.1016/j.puhe.2016.08.007.
190. Facciolà A, Squeri R, Genovese C, Alessi V, La Fauci V. Perception of Rubella risk in pregnancy: an epidemiological survey on a sample of pregnant women. Ann Ig 2019; 31(2 Suppl 1): 65-71. doi: 10.7416/ai.2019.2278.
191. Squeri R, La Fauci V, Picerno IAM, et al. Evaluation of Vaccination Coverages in the Health Care Workers of a University Hospital in Southern Italy. Ann Ig 2019; 31(2 Suppl 1): 13-24. doi:10.7416/ai.2019.2273.
192. Squeri R, Riso R, Facciolà A, et al. Management of two influenza vaccination campaign in health care workers of a university hospital in the south Italy. Ann Ig 2017; 29(3): 223-31. doi: 10.7416/ai.2017.2150. PubMed PMID: 28383614.
193. De Luca F, Aversa T, Alessi L, et al. Thyroid nodules in childhood: indications for biopsy and surgery. Ital J Pediatr 2014; 40: 48. doi: 10.1186/1824-7288-40-48. Review. PubMed PMID: 24887308; PubMed Central PMCID: PMC4046031.

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