Skip to main content
Erschienen in: European Journal of Clinical Microbiology & Infectious Diseases 5/2018

15.02.2018 | Original Article

CC398 Staphylococcus aureus subpopulations in Belgian patients

verfasst von: M. Angeles Argudín, A. Deplano, S. Vandendriessche, M. Dodémont, C. Nonhoff, O. Denis, S. Roisin

Erschienen in: European Journal of Clinical Microbiology & Infectious Diseases | Ausgabe 5/2018

Einloggen, um Zugang zu erhalten

Abstract

Studies based on genome-wide single nucleotide polymorphisms (SNPs) supported the existence of two subpopulations in clonal complex (CC) 398 Staphylococcus aureus: an ancestral human-adapted clade (HC) and an animal-associated clade (AC). In this study, we have investigated the occurrence of genetic markers that allow discrimination of these subpopulations among CC398 isolates collected during 2014 to 2016 from human patients in Belgium. A collection of isolates was investigated by means of spa-typing and 16S-mecA-nuc PCR. CC398 isolates were classified as belonging to the human or the animal clade by using a canonical SNPs PCR and further studied by antimicrobial susceptibility and the presence of toxins, immune evasion cluster (IEC), and resistance genes. A total of 124 (7.8%) human isolates belonged to CC398. They were grouped into HC (n = 58) or AC (n = 66). The genes erm(T), pvl, chp, and scn were predominantly found in HC-CC398, while AC-CC398 isolates carried more frequently than the mecA, erm(C), tet(K), tet(M), and tet(L) genes. Different combinations of gene profiles were observed according to the clade. CC398 isolates from Belgian patients belonged to different subpopulations including typical HC and AC-isolates. Few HC-strains with mecA and AC-isolates harboring IEC were found. CC398 isolates from Belgian patients belonged to different subpopulations including typical HC and AC-isolates, as well as new emerging subpopulations that underline the ability of this lineage to acquire resistance and virulence genes. Further research is needed to evaluate the emergence of these subpopulations in the clinical setting.
Literatur
1.
Zurück zum Zitat Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, Pearson T, Waters AE, Foster JT, Schupp J, Gillece J, Driebe E, Liu CM, Springer B, Zdovc I, Battisti A, Franco A, Zmudzki J, Schwarz S, Butaye P, Jouy E, Pomba C, Porrero MC, Ruimy R, Smith TC, Robinson DA, Weese JS, Arriola CS, Yu F, Laurent F, Keim P, Skov R, Aarestrup FM (2012) Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 3(1):e00305-11 Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, Pearson T, Waters AE, Foster JT, Schupp J, Gillece J, Driebe E, Liu CM, Springer B, Zdovc I, Battisti A, Franco A, Zmudzki J, Schwarz S, Butaye P, Jouy E, Pomba C, Porrero MC, Ruimy R, Smith TC, Robinson DA, Weese JS, Arriola CS, Yu F, Laurent F, Keim P, Skov R, Aarestrup FM (2012) Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 3(1):e00305-11
2.
Zurück zum Zitat McCarthy AJ, van Wamel W, Vandendriessche S, Larsen J, Denis O, Garcia-Graells C, Uhlemann AC, Lowy FD, Skov R, Lindsay JA (2012) Staphylococcus aureus CC398 clade associated with human-to-human transmission. Appl Environ Microbiol 78(24):8845–8848CrossRefPubMedPubMedCentral McCarthy AJ, van Wamel W, Vandendriessche S, Larsen J, Denis O, Garcia-Graells C, Uhlemann AC, Lowy FD, Skov R, Lindsay JA (2012) Staphylococcus aureus CC398 clade associated with human-to-human transmission. Appl Environ Microbiol 78(24):8845–8848CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Stegger M, Liu CM, Larsen J, Soldanova K, Aziz M, Contente-Cuomo T, Petersen A, Vandendriessche S, Jimenez JN, Mammina C, van Belkum A, Salmenlinna S, Laurent F, Skov RL, Larsen AR, Andersen PS, Price LB (2013) Rapid differentiation between livestock-associated and livestock-independent Staphylococcus aureus CC398 clades. PLoS One 8(11):e79645CrossRefPubMedPubMedCentral Stegger M, Liu CM, Larsen J, Soldanova K, Aziz M, Contente-Cuomo T, Petersen A, Vandendriessche S, Jimenez JN, Mammina C, van Belkum A, Salmenlinna S, Laurent F, Skov RL, Larsen AR, Andersen PS, Price LB (2013) Rapid differentiation between livestock-associated and livestock-independent Staphylococcus aureus CC398 clades. PLoS One 8(11):e79645CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Cuny C, Abdelbary M, Layer F, Werner G, Witte W (2015) Prevalence of the immune evasion gene cluster in Staphylococcus aureus CC398. Vet Microbiol 177(1–2):219–223CrossRefPubMed Cuny C, Abdelbary M, Layer F, Werner G, Witte W (2015) Prevalence of the immune evasion gene cluster in Staphylococcus aureus CC398. Vet Microbiol 177(1–2):219–223CrossRefPubMed
5.
Zurück zum Zitat van der Mee-Marquet N, Corvaglia AR, Valentin AS, Hernandez D, Bertrand X, Girard M, Kluytmans J, Donnio PY, Quentin R, Francois P (2013) Analysis of prophages harbored by the human-adapted subpopulation of Staphylococcus aureus CC398. Infect Genet Evol 18:299–308CrossRefPubMed van der Mee-Marquet N, Corvaglia AR, Valentin AS, Hernandez D, Bertrand X, Girard M, Kluytmans J, Donnio PY, Quentin R, Francois P (2013) Analysis of prophages harbored by the human-adapted subpopulation of Staphylococcus aureus CC398. Infect Genet Evol 18:299–308CrossRefPubMed
6.
Zurück zum Zitat Paridaens H, Coussement J, Argudín MA, Delaere B, Huang TD, Glupczynski Y, Denis O (2017) Clinical case of cfr-positive MRSA CC398 in Belgium. Eur J Clin Microbiol Infect Dis 36(8):1527–1529CrossRefPubMed Paridaens H, Coussement J, Argudín MA, Delaere B, Huang TD, Glupczynski Y, Denis O (2017) Clinical case of cfr-positive MRSA CC398 in Belgium. Eur J Clin Microbiol Infect Dis 36(8):1527–1529CrossRefPubMed
7.
Zurück zum Zitat Larsen J, Petersen A, Larsen AR, Sieber RN, Stegger M, Koch A, Aarestrup FM, Price LB, Skov RL, Danish MSG (2017) Emergence of livestock-associated methicillin-resistant Staphylococcus aureus bloodstream infections in Denmark. Clin Infect Dis 65(7):1072–1076CrossRefPubMedCentral Larsen J, Petersen A, Larsen AR, Sieber RN, Stegger M, Koch A, Aarestrup FM, Price LB, Skov RL, Danish MSG (2017) Emergence of livestock-associated methicillin-resistant Staphylococcus aureus bloodstream infections in Denmark. Clin Infect Dis 65(7):1072–1076CrossRefPubMedCentral
8.
Zurück zum Zitat Argudín MA, Dodemont M, Vandendriessche S, Rottiers S, Tribes C, Roisin S, de Mendonca R, Nonhoff C, Deplano A, Denis O (2016) Low occurrence of the new species Staphylococcus argenteus in a Staphylococcus aureus collection of human isolates from Belgium. Eur J Clin Microbiol Infect Dis 35(6):1017–1022CrossRefPubMed Argudín MA, Dodemont M, Vandendriessche S, Rottiers S, Tribes C, Roisin S, de Mendonca R, Nonhoff C, Deplano A, Denis O (2016) Low occurrence of the new species Staphylococcus argenteus in a Staphylococcus aureus collection of human isolates from Belgium. Eur J Clin Microbiol Infect Dis 35(6):1017–1022CrossRefPubMed
11.
Zurück zum Zitat Vandendriessche S, Kadlec K, Schwarz S, Denis O (2011) Methicillin-susceptible Staphylococcus aureus ST398-t571 harbouring the macrolide-lincosamide-streptogramin B resistance gene erm(T) in Belgian hospitals. J Antimicrob Chemother 66(11):2455–2459CrossRefPubMed Vandendriessche S, Kadlec K, Schwarz S, Denis O (2011) Methicillin-susceptible Staphylococcus aureus ST398-t571 harbouring the macrolide-lincosamide-streptogramin B resistance gene erm(T) in Belgian hospitals. J Antimicrob Chemother 66(11):2455–2459CrossRefPubMed
12.
Zurück zum Zitat Vandendriessche S, Vanderhaeghen W, Larsen J, de Mendonca R, Hallin M, Butaye P, Hermans K, Haesebrouck F, Denis O (2014) High genetic diversity of methicillin-susceptible Staphylococcus aureus (MSSA) from humans and animals on livestock farms and presence of SCCmec remnant DNA in MSSA CC398. J Antimicrob Chemother 69(2):355–362CrossRefPubMed Vandendriessche S, Vanderhaeghen W, Larsen J, de Mendonca R, Hallin M, Butaye P, Hermans K, Haesebrouck F, Denis O (2014) High genetic diversity of methicillin-susceptible Staphylococcus aureus (MSSA) from humans and animals on livestock farms and presence of SCCmec remnant DNA in MSSA CC398. J Antimicrob Chemother 69(2):355–362CrossRefPubMed
13.
Zurück zum Zitat Goerge T, Lorenz MB, van Alen S, Hubner NO, Becker K, Kock R (2017) MRSA colonization and infection among persons with occupational livestock exposure in Europe: prevalence, preventive options and evidence. Vet Microbiol 200:6–12CrossRefPubMed Goerge T, Lorenz MB, van Alen S, Hubner NO, Becker K, Kock R (2017) MRSA colonization and infection among persons with occupational livestock exposure in Europe: prevalence, preventive options and evidence. Vet Microbiol 200:6–12CrossRefPubMed
14.
Zurück zum Zitat Benito D, Lozano C, Rezusta A, Ferrer I, Vasquez MA, Ceballos S, Zarazaga M, Revillo MJ, Torres C (2014) Characterization of tetracycline and methicillin resistant Staphylococcus aureus strains in a Spanish hospital: is livestock-contact a risk factor in infections caused by MRSA CC398? Int J Med Microbiol 304(8):1226–1232CrossRefPubMed Benito D, Lozano C, Rezusta A, Ferrer I, Vasquez MA, Ceballos S, Zarazaga M, Revillo MJ, Torres C (2014) Characterization of tetracycline and methicillin resistant Staphylococcus aureus strains in a Spanish hospital: is livestock-contact a risk factor in infections caused by MRSA CC398? Int J Med Microbiol 304(8):1226–1232CrossRefPubMed
15.
Zurück zum Zitat Bootsma MC, Wassenberg MW, Trapman P, Bonten MJ (2011) The nosocomial transmission rate of animal-associated ST398 meticillin-resistant Staphylococcus aureus. J R Soc Interface 8(57):578–584CrossRefPubMed Bootsma MC, Wassenberg MW, Trapman P, Bonten MJ (2011) The nosocomial transmission rate of animal-associated ST398 meticillin-resistant Staphylococcus aureus. J R Soc Interface 8(57):578–584CrossRefPubMed
16.
Zurück zum Zitat Uhlemann AC, Porcella SF, Trivedi S, Sullivan SB, Hafer C, Kennedy AD, Barbian KD, McCarthy AJ, Street C, Hirschberg DL, Lipkin WI, Lindsay JA, DeLeo FR, Lowy FD (2012) Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. MBio 3(2):e00027-12 Uhlemann AC, Porcella SF, Trivedi S, Sullivan SB, Hafer C, Kennedy AD, Barbian KD, McCarthy AJ, Street C, Hirschberg DL, Lipkin WI, Lindsay JA, DeLeo FR, Lowy FD (2012) Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. MBio 3(2):e00027-12
17.
Zurück zum Zitat Benito D, Lozano C, Gomez-Sanz E, Zarazaga M, Torres C (2013) Detection of methicillin-susceptible Staphylococcus aureus ST398 and ST133 strains in gut microbiota of healthy humans in Spain. Microb Ecol 66(1):105–111CrossRefPubMed Benito D, Lozano C, Gomez-Sanz E, Zarazaga M, Torres C (2013) Detection of methicillin-susceptible Staphylococcus aureus ST398 and ST133 strains in gut microbiota of healthy humans in Spain. Microb Ecol 66(1):105–111CrossRefPubMed
18.
Zurück zum Zitat Chroboczek T, Boisset S, Rasigade JP, Tristan A, Bes M, Meugnier H, Vandenesch F, Etienne J, Laurent F (2013) Clonal complex 398 methicillin susceptible Staphylococcus aureus: a frequent unspecialized human pathogen with specific phenotypic and genotypic characteristics. PLoS One 8(11):e68462CrossRefPubMedPubMedCentral Chroboczek T, Boisset S, Rasigade JP, Tristan A, Bes M, Meugnier H, Vandenesch F, Etienne J, Laurent F (2013) Clonal complex 398 methicillin susceptible Staphylococcus aureus: a frequent unspecialized human pathogen with specific phenotypic and genotypic characteristics. PLoS One 8(11):e68462CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Cuny C, Layer F, Kock R, Werner G, Witte W (2013) Methicillin susceptible Staphylococcus aureus (MSSA) of clonal complex CC398, t571 from infections in humans are still rare in Germany. PLoS One 8(12):e83165CrossRefPubMedPubMedCentral Cuny C, Layer F, Kock R, Werner G, Witte W (2013) Methicillin susceptible Staphylococcus aureus (MSSA) of clonal complex CC398, t571 from infections in humans are still rare in Germany. PLoS One 8(12):e83165CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Lekkerkerk WS, van Wamel WJ, Snijders SV, Willems RJ, van Duijkeren E, Broens EM, Wagenaar JA, Lindsay JA, Vos MC (2015) What is the origin of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex 398 isolates from humans without livestock contact? An epidemiological and genetic analysis. J Clin Microbiol 53(6):1836–1841CrossRefPubMedPubMedCentral Lekkerkerk WS, van Wamel WJ, Snijders SV, Willems RJ, van Duijkeren E, Broens EM, Wagenaar JA, Lindsay JA, Vos MC (2015) What is the origin of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex 398 isolates from humans without livestock contact? An epidemiological and genetic analysis. J Clin Microbiol 53(6):1836–1841CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Yu F, Chen Z, Liu C, Zhang X, Lin X, Chi S, Zhou T, Chen Z, Chen X (2008) Prevalence of Staphylococcus aureus carrying Panton-Valentine leukocidin genes among isolates from hospitalised patients in China. Clin Microbiol Infect 14(4):381–384CrossRefPubMed Yu F, Chen Z, Liu C, Zhang X, Lin X, Chi S, Zhou T, Chen Z, Chen X (2008) Prevalence of Staphylococcus aureus carrying Panton-Valentine leukocidin genes among isolates from hospitalised patients in China. Clin Microbiol Infect 14(4):381–384CrossRefPubMed
22.
Zurück zum Zitat Zhao C, Liu Y, Zhao M, Liu Y, Yu Y, Chen H, Sun Q, Chen H, Jiang W, Liu Y, Han S, Xu Y, Chen M, Cao B, Wang H (2012) Characterization of community acquired Staphylococcus aureus associated with skin and soft tissue infection in Beijing: high prevalence of PVL+ ST398. PLoS One 7(6):e38577CrossRefPubMedPubMedCentral Zhao C, Liu Y, Zhao M, Liu Y, Yu Y, Chen H, Sun Q, Chen H, Jiang W, Liu Y, Han S, Xu Y, Chen M, Cao B, Wang H (2012) Characterization of community acquired Staphylococcus aureus associated with skin and soft tissue infection in Beijing: high prevalence of PVL+ ST398. PLoS One 7(6):e38577CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat Welinder-Olsson C, Floren-Johansson K, Larsson L, Oberg S, Karlsson L, Ahren C (2008) Infection with Panton-Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus t034. Emerg Infect Dis 14(8):1271–1272CrossRefPubMedPubMedCentral Welinder-Olsson C, Floren-Johansson K, Larsson L, Oberg S, Karlsson L, Ahren C (2008) Infection with Panton-Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus t034. Emerg Infect Dis 14(8):1271–1272CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Stegger M, Lindsay JA, Sorum M, Gould KA, Skov R (2010) Genetic diversity in CC398 methicillin-resistant Staphylococcus aureus isolates of different geographical origin. Clin Microbiol Infect 16(7):1017–1019CrossRefPubMed Stegger M, Lindsay JA, Sorum M, Gould KA, Skov R (2010) Genetic diversity in CC398 methicillin-resistant Staphylococcus aureus isolates of different geographical origin. Clin Microbiol Infect 16(7):1017–1019CrossRefPubMed
25.
Zurück zum Zitat McCarthy AJ, Witney AA, Gould KA, Moodley A, Guardabassi L, Voss A, Denis O, Broens EM, Hinds J, Lindsay JA (2011) The distribution of mobile genetic elements (MGEs) in MRSA CC398 is associated with both host and country. Genome Biol Evol 3:1164–1174CrossRefPubMedPubMedCentral McCarthy AJ, Witney AA, Gould KA, Moodley A, Guardabassi L, Voss A, Denis O, Broens EM, Hinds J, Lindsay JA (2011) The distribution of mobile genetic elements (MGEs) in MRSA CC398 is associated with both host and country. Genome Biol Evol 3:1164–1174CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Bouiller K, Gbaguidi-Haore H, Hocquet D, Cholley P, Bertrand X, Chirouze C (2016) Clonal complex 398 methicillin-susceptible Staphylococcus aureus bloodstream infections are associated with high mortality. Clin Microbiol Infect 22(5):451–455CrossRefPubMed Bouiller K, Gbaguidi-Haore H, Hocquet D, Cholley P, Bertrand X, Chirouze C (2016) Clonal complex 398 methicillin-susceptible Staphylococcus aureus bloodstream infections are associated with high mortality. Clin Microbiol Infect 22(5):451–455CrossRefPubMed
27.
Zurück zum Zitat Stegger M, Aziz M, Chroboczek T, Price LB, Ronco T, Kiil K, Skov RL, Laurent F, Andersen PS (2013) Genome analysis of Staphylococcus aureus ST291, a double locus variant of ST398, reveals a distinct genetic lineage. PLoS One 8(5):e63008CrossRefPubMedPubMedCentral Stegger M, Aziz M, Chroboczek T, Price LB, Ronco T, Kiil K, Skov RL, Laurent F, Andersen PS (2013) Genome analysis of Staphylococcus aureus ST291, a double locus variant of ST398, reveals a distinct genetic lineage. PLoS One 8(5):e63008CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Haenni M, Chatre P, Boisset S, Carricajo A, Bes M, Laurent F, Madec JY (2011) Staphylococcal nasal carriage in calves: multiresistant Staphylococcus sciuri and immune evasion cluster (IEC) genes in methicillin-resistant Staphylococcus aureus ST398. J Antimicrob Chemother 66(8):1927–1928CrossRefPubMed Haenni M, Chatre P, Boisset S, Carricajo A, Bes M, Laurent F, Madec JY (2011) Staphylococcal nasal carriage in calves: multiresistant Staphylococcus sciuri and immune evasion cluster (IEC) genes in methicillin-resistant Staphylococcus aureus ST398. J Antimicrob Chemother 66(8):1927–1928CrossRefPubMed
29.
Zurück zum Zitat Brennan GI, Abbott Y, Burns A, Leonard F, McManus BA, O'Connell B, Coleman DC, Shore AC (2016) The emergence and spread of multiple livestock-associated clonal complex 398 methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains among animals and humans in the Republic of Ireland, 2010–2014. PLoS One 11(2):e0149396CrossRefPubMedPubMedCentral Brennan GI, Abbott Y, Burns A, Leonard F, McManus BA, O'Connell B, Coleman DC, Shore AC (2016) The emergence and spread of multiple livestock-associated clonal complex 398 methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains among animals and humans in the Republic of Ireland, 2010–2014. PLoS One 11(2):e0149396CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Pérez-Moreno MO, Centelles-Serrano MJ, Nogales-Lopez J, Domenech-Spanedda MF, Lozano C, Torres C (2016) Unusual presence of the immune evasion gene cluster in livestock-associated MRSA of lineage CC398 causing peridural and psoas abscesses in a poultry farmer. Enferm Infecc Microbiol Clin 35(10):651–654CrossRefPubMed Pérez-Moreno MO, Centelles-Serrano MJ, Nogales-Lopez J, Domenech-Spanedda MF, Lozano C, Torres C (2016) Unusual presence of the immune evasion gene cluster in livestock-associated MRSA of lineage CC398 causing peridural and psoas abscesses in a poultry farmer. Enferm Infecc Microbiol Clin 35(10):651–654CrossRefPubMed
31.
Zurück zum Zitat Spoor LE, McAdam PR, Weinert LA, Rambaut A, Hasman H, Aarestrup FM, Kearns AM, Larsen AR, Skov RL, Fitzgerald JR (2013) Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus. MBio 4(4):e00356-13 Spoor LE, McAdam PR, Weinert LA, Rambaut A, Hasman H, Aarestrup FM, Kearns AM, Larsen AR, Skov RL, Fitzgerald JR (2013) Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus. MBio 4(4):e00356-13
32.
Zurück zum Zitat Jung P, Abdelbary MM, Kraushaar B, Fetsch A, Geisel J, Herrmann M, Witte W, Cuny C, Bischoff M (2017) Impact of bacteriophage Saint3 carriage on the immune evasion capacity and hemolytic potential of Staphylococcus aureus CC398. Vet Microbiol 200:46–51CrossRefPubMed Jung P, Abdelbary MM, Kraushaar B, Fetsch A, Geisel J, Herrmann M, Witte W, Cuny C, Bischoff M (2017) Impact of bacteriophage Saint3 carriage on the immune evasion capacity and hemolytic potential of Staphylococcus aureus CC398. Vet Microbiol 200:46–51CrossRefPubMed
Metadaten
Titel
CC398 Staphylococcus aureus subpopulations in Belgian patients
verfasst von
M. Angeles Argudín
A. Deplano
S. Vandendriessche
M. Dodémont
C. Nonhoff
O. Denis
S. Roisin
Publikationsdatum
15.02.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Clinical Microbiology & Infectious Diseases / Ausgabe 5/2018
Print ISSN: 0934-9723
Elektronische ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-018-3205-y

Weitere Artikel der Ausgabe 5/2018

European Journal of Clinical Microbiology & Infectious Diseases 5/2018 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.