Abstract
While there is an abundance of data on the epidemiology and molecular typing of Staphylococcus aureus, especially those carrying Panton–Valentine leucocidin (PVL) genes or mecA from Western Europe, Northern America and Australia, comparably few studies target African strains. In this study, we characterised genes associated with virulence and resistance, as well the phylogenetic background of S. aureus from healthy carriers and outpatients in Gabon. In total, 103 isolates from 96 study participants were characterised. Seventy-nine isolates originated from throat swabs and 24 isolates from skin lesions. Three isolates carried mecA, although only one, belonging to CC8-MRSA-IV [PVL+] ‘USA300’, was found to be phenotypically oxacillin-resistant; two CC88-MRSA-IV isolates appeared to be oxacillin-susceptible. PVL genes were common, with a total of 44 isolates (43 %) found to be PVL-positive. CC15-MSSA [PVL+] (n = 29) and CC152-MSSA [PVL+] (n = 9) were the predominant clones among the PVL-positive isolates. Among PVL-negative isolates, CC5-MSSA (n = 12), CC101-MSSA (n = 10) and CC15 (n = 9) were the most frequent. A hitherto undescribed multilocus sequence type of S. schweitzeri was detected twice in unrelated patients. The data emphasise a need for further studies on the role of PVL in African populations and the clinical significance of S. schweitzeri.
Similar content being viewed by others
References
Hiramatsu K, Cui L, Kuroda M, Ito T (2001) The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 9(10):486–493
Kaneko J, Kamio Y (2004) Bacterial two-component and hetero-heptameric pore-forming cytolytic toxins: structures, pore-forming mechanism, and organization of the genes. Biosci Biotechnol Biochem 68(5):981–1003
Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339(8):520–532. doi:10.1056/NEJM199808203390806
Lowy FD (2013) Methicillin-resistant Staphylococcus aureus: where is it coming from and where is it going? JAMA Intern Med 173(21):1978–1979. doi:10.1001/jamainternmed.2013.8277
Schlievert PM, Shands KN, Dan BB, Schmid GP, Nishimura RD (1981) Identification and characterization of an exotoxin from Staphylococcus aureus associated with toxic-shock syndrome. J Infect Dis 143(4):509–516
Waldvogel FA (1995) Staphylococcus aureus (including toxic shock syndrome). In: Mandell, Douglas and Bennett’s principles and practice of infectious diseases. Churchill Livingstone, New York, Edinburgh, London, Melbourne, and Tokyo
Genestier AL, Michallet MC, Prévost G, Bellot G, Chalabreysse L, Peyrol S, Thivolet F, Etienne J, Lina G, Vallette FM, Vandenesch F, Genestier L (2005) Staphylococcus aureus Panton–Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils. J Clin Invest 115(11):3117–3127
Cribier B, Prévost G, Couppie P, Finck-Barbançon V, Grosshans E, Piémont Y (1992) Staphylococcus aureus leukocidin: a new virulence factor in cutaneous infections? An epidemiological and experimental study. Dermatology 185(3):175–180
Durupt F, Mayor L, Bes M, Reverdy ME, Vandenesch F, Thomas L, Etienne J (2007) Prevalence of Staphylococcus aureus toxins and nasal carriage in furuncles and impetigo. Br J Dermatol 157(6):1161–1167
Issartel B, Tristan A, Lechevallier S, Bruyère F, Lina G, Garin B, Lacassin F, Bes M, Vandenesch F, Etienne J (2005) Frequent carriage of Panton–Valentine leucocidin genes by Staphylococcus aureus isolates from surgically drained abscesses. J Clin Microbiol 43(7):3203–3207
Iwatsuki K, Yamasaki O, Morizane S, Oono T (2006) Staphylococcal cutaneous infections: invasion, evasion and aggression. J Dermatol Sci 42(3):203–214
König B, Prévost G, König W (1997) Composition of staphylococcal bi-component toxins determines pathophysiological reactions. J Med Microbiol 46(6):479–485
Yamasaki O, Kaneko J, Morizane S, Akiyama H, Arata J, Narita S, Chiba J, Kamio Y, Iwatsuki K (2005) The association between Staphylococcus aureus strains carrying Panton–Valentine leukocidin genes and the development of deep-seated follicular infection. Clin Infect Dis 40(3):381–385
Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, Bes M, Vandenesch F, Piémont Y, Brousse N, Floret D, Etienne J (2002) Association between Staphylococcus aureus strains carrying gene for Panton–Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 359(9308):753–759
Abdulgader SM, Shittu AO, Nicol MP, Kaba M (2015) Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Africa: a systematic review. Front Microbiol 6:348. doi:10.3389/fmicb.2015.00348
Conceição T, Coelho C, Santos Silva I, de Lencastre H, Aires-de-Sousa M (2016) Methicillin-resistant Staphylococcus aureus in the community in Luanda, Angola: blurred boundaries with the hospital setting. Microb Drug Resist 22(1):22–27. doi:10.1089/mdr.2015.0236
Schaumburg F, Pauly M, Anoh E, Mossoun A, Wiersma L, Schubert G, Flammen A, Alabi AS, Muyembe-Tamfum JJ, Grobusch MP, Karhemere S, Akoua-Koffi C, Couacy-Hymann E, Kremsner PG, Mellmann A, Becker K, Leendertz FH, Peters G (2015) Staphylococcus aureus complex from animals and humans in three remote African regions. Clin Microbiol Infect 21(4):345.e1–345.e8. doi:10.1016/j.cmi.2014.12.001
Tong SY, Schaumburg F, Ellington MJ, Corander J, Pichon B, Leendertz F, Bentley SD, Parkhill J, Holt DC, Peters G, Giffard PM (2015) Novel staphylococcal species that form part of a Staphylococcus aureus-related complex: the non-pigmented Staphylococcus argenteus sp. nov. and the non-human primate-associated Staphylococcus schweitzeri sp. nov. Int J Syst Evol Microbiol 65(Pt 1):15–22. doi:10.1099/ijs.0.062752-0
Egyir B, Guardabassi L, Esson J, Nielsen SS, Newman MJ, Addo KK, Larsen AR (2014) Insights into nasal carriage of Staphylococcus aureus in an urban and a rural community in Ghana. PLoS One 9(4):e96119. doi:10.1371/journal.pone.0096119
Egyir B, Guardabassi L, Nielsen SS, Larsen J, Addo KK, Newman MJ, Larsen AR (2013) Prevalence of nasal carriage and diversity of Staphylococcus aureus among inpatients and hospital staff at Korle Bu Teaching Hospital, Ghana. J Glob Antimicrob Resist 1(4):189–193. doi:10.1016/j.jgar.2013.05.006
Egyir B, Guardabassi L, Sørum M, Nielsen SS, Kolekang A, Frimpong E, Addo KK, Newman MJ, Larsen AR (2014) Molecular epidemiology and antimicrobial susceptibility of clinical Staphylococcus aureus from healthcare institutions in Ghana. PLoS One 9(2):e89716. doi:10.1371/journal.pone.0089716
Aiken AM, Mutuku IM, Sabat AJ, Akkerboom V, Mwangi J, Scott JAG, Morpeth SC, Friedrich AW, Grundmann H (2014) Carriage of Staphylococcus aureus in Thika Level 5 Hospital, Kenya: a cross-sectional study. Antimicrob Resist Infect Control 3(1):1–7. doi:10.1186/2047-2994-3-22
Ayepola OO, Olasupo NA, Egwari LO, Becker K, Schaumburg F (2015) Molecular characterization and antimicrobial susceptibility of Staphylococcus aureus isolates from clinical infection and asymptomatic carriers in Southwest Nigeria. PLoS One 10(9):e0137531. doi:10.1371/journal.pone.0137531
Shittu AO, Oyedara O, Okon K, Raji A, Peters G, von Müller L, Schaumburg F, Herrmann M, Ruffing U (2015) An assessment on DNA microarray and sequence-based methods for the characterization of methicillin-susceptible Staphylococcus aureus from Nigeria. Front Microbiol 6:1160. doi:10.3389/fmicb.2015.01160
Okon KO, Basset P, Uba A, Lin J, Oyawoye B, Shittu AO, Blanc DS (2009) Cooccurrence of predominant Panton–Valentine leukocidin-positive sequence type (ST) 152 and multidrug-resistant ST 241 Staphylococcus aureus clones in Nigerian hospitals. J Clin Microbiol 47(9):3000–3003. doi:10.1128/JCM.01119-09
Akobi B, Aboderin O, Sasaki T, Shittu A (2012) Characterization of Staphylococcus aureus isolates from faecal samples of the straw-coloured fruit bat (Eidolon helvum) in Obafemi Awolowo University (OAU), Nigeria. BMC Microbiol 12:279. doi:10.1186/1471-2180-12-279
Ruimy R, Maiga A, Armand-Lefevre L, Maiga I, Diallo A, Koumaré AK, Ouattara K, Soumaré S, Gaillard K, Lucet JC, Andremont A, Feil EJ (2008) The carriage population of Staphylococcus aureus from Mali is composed of a combination of pandemic clones and the divergent Panton–Valentine leukocidin-positive genotype ST152. J Bacteriol 190(11):3962–3968
Fall C, Seck A, Richard V, Ndour M, Sembene M, Laurent F, Breurec S (2012) Epidemiology of Staphylococcus aureus in pigs and farmers in the largest farm in Dakar, Senegal. Foodborne Pathog Dis 9(10):962–965. doi:10.1089/fpd.2012.1197
Rasigade JP, Trouillet-Assant S, Breurec S, Antri K, Lina G, Bes M, Tristan A, Badiou C, Bernelin M, Fall C, Ramdani-Bouguessa N, Etienne J, Vandenesch F, Laurent F (2015) The levels of antibodies to Panton–Valentine leukocidin (PVL) vary with PVL prevalence along a north-to-south gradient. Eur J Clin Microbiol Infect Dis 34(5):927–933. doi:10.1007/s10096-014-2307-4
Oosthuysen WF, Orth H, Lombard CJ, Sinha B, Wasserman E (2014) Population structure analyses of Staphylococcus aureus at Tygerberg Hospital, South Africa, reveals a diverse population, a high prevalence of Panton–Valentine leukocidin genes, and unique local methicillin-resistant S. aureus clones. Clin Microbiol Infect 20(7):652–659. doi:10.1111/1469-0691.12452
Monecke S, Müller E, Buechler J, Rejman J, Stieber B, Akpaka PE, Bandt D, Burris R, Coombs G, Hidalgo-Arroyo GA, Hughes P, Kearns A, Abós SM, Pichon B, Skakni L, Söderquist B, Ehricht R (2013) Rapid detection of Panton–Valentine leukocidin in Staphylococcus aureus cultures by use of a lateral flow assay based on monoclonal antibodies. J Clin Microbiol 51(2):487–495. doi:10.1128/JCM.02285-12
Schaumburg F, Ngoa UA, Kösters K, Köck R, Adegnika AA, Kremsner PG, Lell B, Peters G, Mellmann A, Becker K (2011) Virulence factors and genotypes of Staphylococcus aureus from infection and carriage in Gabon. Clin Microbiol Infect 17:1507–1513
Ateba Ngoa U, Schaumburg F, Adegnika AA, Kösters K, Möller T, Fernandes JF, Alabi A, Issifou S, Becker K, Grobusch MP, Kremsner PG, Lell B (2012) Epidemiology and population structure of Staphylococcus aureus in various population groups from a rural and semi urban area in Gabon, Central Africa. Acta Trop 124(1):42–47. doi:10.1016/j.actatropica.2012.06.005
Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, Chow H, Ip M, Jatzwauk L, Jonas D, Kadlec K, Kearns A, Laurent F, O’Brien FG, Pearson J, Ruppelt A, Schwarz S, Scicluna E, Slickers P, Tan H-L, Weber S, Ehricht R (2011) A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One 6(4):e17936
Monecke S, Slickers P, Ehricht R (2008) Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol 53:237–251
Monecke S, Gavier-Widen D, Mattsson R, Rangstrup-Christensen L, Lazaris A, Coleman DC, Shore AC, Ehricht R (2013) Detection of mecC-positive Staphylococcus aureus (CC130-MRSA-XI) in diseased European hedgehogs (Erinaceus europaeus) in Sweden. PLoS One 8(6):e66166. doi:10.1371/journal.pone.0066166
Bélard S, Toepfner N, Arnold B, Alabi AS, Berner R (2015) beta-Hemolytic streptococcal throat carriage and tonsillopharyngitis: a cross-sectional prevalence study in Gabon, Central Africa. Infection 43(2):177–183. doi:10.1007/s15010-014-0709-y
Conceição T, Santos Silva I, de Lencastre H, Aires-de-Sousa M (2014) Staphylococcus aureus nasal carriage among patients and health care workers in São Tomé and Príncipe. Microb Drug Resist 20(1):57–66. doi:10.1089/mdr.2013.0136
Shittu A, Oyedara O, Abegunrin F, Okon K, Raji A, Taiwo S, Ogunsola F, Onyedibe K, Elisha G (2012) Characterization of methicillin-susceptible and -resistant staphylococci in the clinical setting: a multicentre study in Nigeria. BMC Infect Dis 12:286. doi:10.1186/1471-2334-12-286
Phaku P, Lebughe M, Strauß L, Peters G, Herrmann M, Mumba D, Mellmann A, Muyembe-Tamfum J-J, Schaumburg F (2016) Unveiling the molecular basis of antimicrobial resistance in Staphylococcus aureus from the Democratic Republic of the Congo using whole genome sequencing. Clin Microbiol Infect. doi:10.1016/j.cmi.2016.04.009
Conceição T, Coelho C, de Lencastre H, Aires-de-Sousa M (2015) Frequent occurrence of oxacillin-susceptible mecA-positive Staphylococcus aureus (OS-MRSA) strains in two African countries. J Antimicrob Chemother 70(12):3200–3204. doi:10.1093/jac/dkv261
Monecke S, Baier V, Coombs GW, Slickers P, Ziegler A, Ehricht R (2013) Genome sequencing and molecular characterisation of Staphylococcus aureus ST772-MRSA-V, “Bengal Bay Clone”. BMC Res Notes 6(1):1–7. doi:10.1186/1756-0500-6-548
Prabhakara S, Khedkar S, Shambat SM, Srinivasan R, Basu A, Norrby-Teglund A, Seshasayee ASN, Arakere G (2013) Genome sequencing unveils a novel sea enterotoxin-carrying PVL phage in Staphylococcus aureus ST772 from India. PLoS One 8(3):e60013. doi:10.1371/journal.pone.0060013
Luedicke C, Slickers P, Ehricht R, Monecke S (2010) Molecular fingerprinting of Staphylococcus aureus from bone and joint infections. Eur J Clin Microbiol Infect Dis 29(4):457–463
Monecke S, Stieber B, Roberts R, Akpaka PE, Slickers P, Ehricht R (2014) Population structure of Staphylococcus aureus from Trinidad & Tobago. PLoS One 9(2):e89120. doi:10.1371/journal.pone.0089120
Sakwinska O, Kuhn G, Balmelli C, Francioli P, Giddey M, Perreten V, Riesen A, Zysset F, Blanc DS, Moreillon P (2009) Genetic diversity and ecological success of Staphylococcus aureus strains colonizing humans. Appl Environ Microbiol 75(1):175–183
Breurec S, Zriouil SB, Fall C, Boisier P, Brisse S, Djibo S, Etienne J, Fonkoua MC, Perrier-Gros-Claude JD, Pouillot R, Ramarokoto CE, Randrianirina F, Tall A, Thiberge JM; Working Group on Staphylococcus aureus infections, Laurent F, Garin B (2011) Epidemiology of methicillin-resistant Staphylococcus aureus lineages in five major African towns: emergence and spread of atypical clones. Clin Microbiol Infect 17(2):160–165. doi:10.1111/j.1469-0691.2010.03219.x
Schaumburg F, Alabi AS, Mombo-Ngoma G, Kaba H, Zoleko RM, Diop DA, Mackanga JR, Basra A, Gonzalez R, Menendez C, Grobusch MP, Kremsner PG, Köck R, Peters G, Ramharter M, Becker K (2014) Transmission of Staphylococcus aureus between mothers and infants in an African setting. Clin Microbiol Infect 20(6):O390–O396. doi:10.1111/1469-0691.12417
Egyir B, Guardabassi L, Monecke S, Addo KK, Newman MJ, Larsen AR (2015) Methicillin-resistant Staphylococcus aureus strains from Ghana include USA300. J Glob Antimicrob Resist 3(1):26–30. doi:10.1016/j.jgar.2014.11.006
Lowder BV, Guinane CM, Ben Zakour NL, Weinert LA, Conway-Morris A, Cartwright RA, Simpson AJ, Rambaut A, Nübel U, Fitzgerald JR (2009) Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A 106(46):19545–19550
Monecke S, Ruppelt A, Wendlandt S, Schwarz S, Slickers P, Ehricht R, Jäckel SC (2013) Genotyping of Staphylococcus aureus isolates from diseased poultry. Vet Microbiol 162(2–4):806–812. doi:10.1016/j.vetmic.2012.10.018
Wendlandt S, Kadlec K, Feßler AT, Monecke S, Ehricht R, van de Giessen AW, Hengeveld PD, Huijsdens X, Schwarz S, van Duijkeren E (2013) Resistance phenotypes and genotypes of methicillin-resistant Staphylococcus aureus isolates from broiler chickens at slaughter and abattoir workers. J Antimicrob Chemother 68(11):2458–2463. doi:10.1093/jac/dkt239
Sung JM-L, Lloyd DH, Lindsay JA (2008) Staphylococcus aureus host specificity: comparative genomics of human versus animal isolates by multi-strain microarray. Microbiology 154(Pt 7):1949–1959. doi:10.1099/mic.0.2007/015289-0
Smyth DS, Feil EJ, Meaney WJ, Hartigan PJ, Tollersrud T, Fitzgerald JR, Enright MC, Smyth CJ (2009) Molecular genetic typing reveals further insights into the diversity of animal-associated Staphylococcus aureus. J Med Microbiol 58(Pt 10):1343–1353
Schaumburg F, Gast B, Sannon H, Mellmann A, Becker K (2015) Is Africa the origin of major Haitian Staphylococcus aureus lineages? Int J Infect Dis 34:1–2. doi:10.1016/j.ijid.2015.02.012
Leiva Peláez O, Stojanov M, Zayas Tamayo AM, Barreras García G, González Aleman M, Martínez Ceballos L, Muñoz del Campo JL, Bello Rodríguez O, Gonzalez Mesa L, Blanc DS (2015) Molecular epidemiology of methicillin-resistant Staphylococcus aureus from 4 Cuban hospitals. Diagn Microbiol Infect Dis 81(1):1–3. doi:10.1016/j.diagmicrobio.2014.10.012
Jimenez-Truque N, Saye EJ, Thomsen I, Herrera ML, Creech CB (2014) Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Costa Rican Children. Pediatr Infect Dis J 33(7):e180–e182. doi:10.1097/inf.0000000000000291
McNeill WH (1998) Plagues and peoples. Anchor, New York
Andernach IE, Nolte C, Pape JW, Muller CP (2009) Slave trade and hepatitis B virus genotypes and subgenotypes in Haiti and Africa. Emerg Infect Dis 15(8):1222–1228. doi:10.3201/eid1508.081642
Amissah NA, Chlebowicz MA, Ablordey A, Sabat AJ, Tetteh CS, Prah I, van der Werf TS, Friedrich AW, van Dijl JM, Rossen JW, Stienstra Y (2015) Molecular characterization of Staphylococcus aureus isolates transmitted between patients with buruli ulcer. PLoS Negl Trop Dis 9(9):e0004049. doi:10.1371/journal.pntd.0004049
Acknowledgements
The authors acknowledge Dr. H. Hotzel of the Institute of Bacterial Infections and Zoonoses (IBIZ), Friedrich Loeffler Institute (FLI), Jena, for help with performing MLST as well as Prof. E. Jacobs (Dresden) and Dr. R Ehricht (Jena) for their support. We thank the medical and laboratory staff at the CERMEL as well as the participating patients for their cooperation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding information
The clinical part of this work was supported by the German Society for Paediatric Infectious Diseases (Deutsche Gesellschaft für Pädiatrische Infektiologie), grant number DGPI07/2012. For the molecular studies, there was no external funding. Each of the participating institutions covered the costs of experiments performed in the respective institutions, as well as granted the time needed to perform this study.
Conflict of interest
Stefan Monecke is an employee of Alere Technologies GmbH, Jena, Germany, the company that manufactures the microarrays used for this study. The other authors do not declare conflicts of interest.
Ethical approval and informed consent
The study was approved by the CERMEL Institutional Review Board. Informed consent was obtained from all participants prior to any study procedure; for minors, a parent or legal guardian provided written consent.
Additional information
K. V. Okuda, N. Toepfner and Stefan Monecke contributed equally to the study.
Rights and permissions
About this article
Cite this article
Okuda, K.V., Toepfner, N., Alabi, A.S. et al. Molecular epidemiology of Staphylococcus aureus from Lambaréné, Gabon. Eur J Clin Microbiol Infect Dis 35, 1963–1973 (2016). https://doi.org/10.1007/s10096-016-2748-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10096-016-2748-z