{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,19]],"date-time":"2026-09-19T00:14:14Z","timestamp":1789776854120,"version":"4.0.1"},"reference-count":39,"publisher":"IWA Publishing","issue":"4","content-domain":{"domain":["iwaponline.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2017,8,1]]},"abstract":"<jats:p>The objective was to characterize Staphylococcus aureus isolated from two wastewater treatment plants (WWTPs) located in Tunis City (Tunisia), during the period 2014\u20132015. Genetic lineages, antibiotic resistance mechanisms and virulence factors were determined for the recovered isolates. S. aureus isolates were recovered from 12 of the 62 wastewater samples tested (19.35%), and one isolate\/sample was characterized, all of them being methicillin-susceptible (MSSA). Six spa types (t587, t674, t224, t127, t701 and t1534) were found among the 12 isolates, and the spa-t587, associated with the new sequence type ST3245, was the most predominant one (7 isolates). The remaining isolates were assigned to five clonal complexes (CC5, CC97, CC1, CC6 and CC522) according to the sequence-type determined and\/or the spa-type detected. S. aureus isolates were ascribed to agrI (n = 3), agrII (n = 7) and agrIII (n = 1); however, one isolate was non-typeable. S. aureus showed resistance to (number of isolates): penicillin (12), erythromycin (7), tetracycline (one) and clindamycin (one). Among the virulence factors investigated, only one isolate harboured the tst gene, encoding the TSST-1 (toxic shock syndrome toxin 1). Despite the low number of studied isolates, the present study reports the occurrence of both human- and animal-associated S. aureus clonal complexes in WWTPs in Tunisia.<\/jats:p>","DOI":"10.2166\/wh.2017.258","type":"journal-article","created":{"date-parts":[[2017,4,6]],"date-time":"2017-04-06T00:25:38Z","timestamp":1491438338000},"page":"638-643","update-policy":"https:\/\/doi.org\/10.2166\/iwapcrossmarkpolicypage","source":"Crossref","is-referenced-by-count":34,"title":["Staphylococcus aureus isolated from wastewater treatment plants in Tunisia: occurrence of human and animal associated lineages"],"prefix":"10.2166","volume":"15","author":[{"given":"Meriam","family":"Ben Said","sequence":"first","affiliation":[{"name":"Universit\u00e9 de Tunis El Manar, Institut de la Recherche V\u00e9t\u00e9rinaire de Tunisie, 20 rue Jebel Lakhdhar, Bab Saadoun, Tunis 1006, Tunisia"},{"name":"Laboratoire de Traitement des Eaux Us\u00e9es, Centre de Recherche et des Technologies des Eaux (CERTE), Technopoles Borj-C\u00e9dria, BP 273, 8020 Soliman, Tunisia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed Salah","family":"Abbassi","sequence":"first","affiliation":[{"name":"Universit\u00e9 de Tunis El Manar, Institut de la Recherche V\u00e9t\u00e9rinaire de Tunisie, 20 rue Jebel Lakhdhar, Bab Saadoun, Tunis 1006, Tunisia"},{"name":"Universit\u00e9 de Tunis El Manar, Facult\u00e9 de M\u00e9decine de Tunis, Laboratoire de r\u00e9sistance aux antibiotiques LR99ES09, Tunisie"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paula","family":"G\u00f3mez","sequence":"first","affiliation":[{"name":"\u00c1rea de Bioqu\u00edmica y Biolog\u00eda Molecular, Universidad de La Rioja, 26006 Logro\u00f1o, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura","family":"Ruiz-Ripa","sequence":"first","affiliation":[{"name":"\u00c1rea de Bioqu\u00edmica y Biolog\u00eda Molecular, Universidad de La Rioja, 26006 Logro\u00f1o, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Senda","family":"Sghaier","sequence":"first","affiliation":[{"name":"Universit\u00e9 de Tunis El Manar, Institut de la Recherche V\u00e9t\u00e9rinaire de Tunisie, 20 rue Jebel Lakhdhar, Bab Saadoun, Tunis 1006, Tunisia"},{"name":"Laboratoire de Traitement des Eaux Us\u00e9es, Centre de Recherche et des Technologies des Eaux (CERTE), Technopoles Borj-C\u00e9dria, BP 273, 8020 Soliman, Tunisia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chourouk","family":"Ibrahim","sequence":"first","affiliation":[{"name":"Laboratoire de Traitement des Eaux Us\u00e9es, Centre de Recherche et des Technologies des Eaux (CERTE), Technopoles Borj-C\u00e9dria, BP 273, 8020 Soliman, Tunisia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carmen","family":"Torres","sequence":"first","affiliation":[{"name":"\u00c1rea de Bioqu\u00edmica y Biolog\u00eda Molecular, Universidad de La Rioja, 26006 Logro\u00f1o, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abdennaceur","family":"Hassen","sequence":"first","affiliation":[{"name":"Laboratoire de Traitement des Eaux Us\u00e9es, Centre de Recherche et des Technologies des Eaux (CERTE), Technopoles Borj-C\u00e9dria, BP 273, 8020 Soliman, Tunisia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"945","published-online":{"date-parts":[[2017,4,5]]},"reference":[{"key":"2020032616150849800_JWH-D-16-00258C1","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1007\/s10096-010-1109-6","article-title":"Nasal carriage of Staphylococcus aureus in healthy humans with different levels of contact with animal in Tunisia: genetic lineage, methicillin resistance, and virulence factors","volume":"30","author":"Ben Slama","year":"2011","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"2020032616150849800_JWH-D-16-00258C2","doi-asserted-by":"crossref","first-page":"1244","DOI":"10.1111\/j.1365-2672.2009.04515.x","article-title":"Methicillin resistant Staphylococcus aureus (MRSA) in municipal wastewater: an uncharted threat?","volume":"108","author":"B\u00f6rjesson","year":"2010","journal-title":"J. Appl. Microbiol."},{"key":"2020032616150849800_JWH-D-16-00258C3","unstructured":"CLSI (Clinical Laboratory Standards Institute)\n          2015\n          Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Information Supplement. M100-S25. National Committee for Clinical Laboratory Standards, Wayne, PA, USA."},{"key":"2020032616150849800_JWH-D-16-00258C4","volume-title":"Multiplex PCR for the Detection of the MecA Gene and the Identification of Staphylococcus Aureus","author":"CRL-AR (Community Reference Laboratory for Antimicrobial Resistance)","year":"2009"},{"key":"2020032616150849800_JWH-D-16-00258C5","doi-asserted-by":"crossref","first-page":"521","DOI":"10.3390\/antibiotics4040521","article-title":"Livestock-associated MRSA: the impact on humans","volume":"4","author":"Cuny","year":"2015","journal-title":"Antibiotics"},{"key":"2020032616150849800_JWH-D-16-00258C6","doi-asserted-by":"crossref","first-page":"1008","DOI":"10.1128\/JCM.38.3.1008-1015.2000","article-title":"Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus","volume":"38","author":"Enright","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"2020032616150849800_JWH-D-16-00258C7","doi-asserted-by":"crossref","first-page":"2607","DOI":"10.1016\/S0043-1354(01)00475-4","article-title":"Fecal coliform removal in wastewater treatment plants studied by plate counts and enzymatic methods","volume":"3","author":"George","year":"2002","journal-title":"Water Res."},{"key":"2020032616150849800_JWH-D-16-00258C8","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/j.vetmic.2011.11.009","article-title":"Prevalence, antibiotic resistance, virulence traits and genetic lineages of Staphylococcus aureus in healthy sheep in Tunisia","volume":"156","author":"Gharsa","year":"2012","journal-title":"Vet. Microbiol."},{"key":"2020032616150849800_JWH-D-16-00258C9","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1186\/1746-6148-8-203","article-title":"High diversity of genetic lineages and virulence genes in nasal Staphylococcus aureus isolates from donkeys destined to food consumption in Tunisia with predominance of the ruminant associated CC133 lineage","volume":"8","author":"Gharsa","year":"2012","journal-title":"BMC Vet. Res."},{"key":"2020032616150849800_JWH-D-16-00258C10","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1089\/vbz.2014.1655","article-title":"Molecular characterization of Staphylococcus aureus from nasal samples of healthy farm animals and pets in Tunisia","volume":"15","author":"Gharsa","year":"2015","journal-title":"Vector Borne Zoonotic Dis."},{"key":"2020032616150849800_JWH-D-16-00258C11","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.envpol.2016.01.038","article-title":"Characterization of Staphylococci in urban wastewater treatment plants in Spain, with detection of methicillin-resistant Staphylococcus aureus ST398","volume":"212","author":"G\u00f3mez","year":"2016","journal-title":"Environ. Pollut."},{"key":"2020032616150849800_JWH-D-16-00258C12","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1089\/fpd.2010.0610","article-title":"Detection, molecular characterization, and clonal diversity of methicillin-resistant Staphylococcus aureus CC398 and CC97 in Spanish slaughter pigs of different age groups","volume":"7","author":"G\u00f3mez-Sanz","year":"2010","journal-title":"Foodborne Pathog. Dis."},{"key":"2020032616150849800_JWH-D-16-00258C13","doi-asserted-by":"crossref","first-page":"5442","DOI":"10.1128\/JCM.41.12.5442-5448.2003","article-title":"Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management","volume":"41","author":"Harmsen","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"2020032616150849800_JWH-D-16-00258C14","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1016\/j.vetmic.2009.09.025","article-title":"Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry","volume":"141","author":"Hasman","year":"2010","journal-title":"Vet. Microbiol."},{"key":"2020032616150849800_JWH-D-16-00258C15","doi-asserted-by":"crossref","first-page":"2130","DOI":"10.1128\/JCM.01940-09","article-title":"Genetic variation among Staphylococcus aureus strains from bovine milk and their relevance to methicillin-resistant isolates from humans","volume":"48","author":"Hata","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"2020032616150849800_JWH-D-16-00258C16","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1128\/IAI.70.2.631-641.2002","article-title":"Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease","volume":"70","author":"Jarraud","year":"2002","journal-title":"Infect. Immun."},{"key":"2020032616150849800_JWH-D-16-00258C17","doi-asserted-by":"crossref","first-page":"1020","DOI":"10.1111\/j.1469-0691.2010.03367.x","article-title":"Molecular analysis of community-acquired methicillin-susceptible and resistant Staphylococcus aureus isolates recovered from bacteraemia and osteomyelitis infections in children from Tunisia","volume":"17","author":"Kechrid","year":"2010","journal-title":"Clin. Microbiol. Infect."},{"key":"2020032616150849800_JWH-D-16-00258C18","doi-asserted-by":"crossref","first-page":"4134","DOI":"10.1007\/s10661-014-4134-6","article-title":"Staphylococcus aureus in nasal carriage, food, wastewater and paper currency in Jalandhar city (north-western), an Indian state of Punjab","volume":"187","author":"Kumar","year":"2015","journal-title":"Environ. Assess."},{"key":"2020032616150849800_JWH-D-16-00258C19","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1093\/cid\/cis1205","article-title":"CC9 livestock-associated Staphylococcus aureus emerges in bloodstream infection in French patients unconnected with animal farming","volume":"56","author":"Lamamy","year":"2013","journal-title":"Clin. Infect. Dis."},{"key":"2020032616150849800_JWH-D-16-00258C20","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1086\/313461","article-title":"Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia","volume":"29","author":"Lina","year":"1999","journal-title":"Clin. Infect. Dis."},{"key":"2020032616150849800_JWH-D-16-00258C21","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1172\/JCI18535","article-title":"Antimicrobial resistance: the example of Staphylococcus aureus","volume":"111","author":"Lowy","year":"2003","journal-title":"J. Clin. Invest."},{"key":"2020032616150849800_JWH-D-16-00258C22","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1089\/vbz.2010.0226","article-title":"Skin lesion by methicillin-resistant Staphylococcus aureus ST398-t1451 in a Spanish pig farmer: possible transmission from animals to humans","volume":"11","author":"Lozano","year":"2011","journal-title":"Vector Borne Zoonotic Dis."},{"key":"2020032616150849800_JWH-D-16-00258C23","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1016\/j.ijantimicag.2012.06.009","article-title":"Identification of novel vga(A)-carrying plasmids and a tn5406-like transposon in methicillin-resistant Staphylococcus aureus and Staphylococcus epidermidis of human and animal origin","volume":"40","author":"Lozano","year":"2012","journal-title":"Int. J. Antimicrob. Agents"},{"key":"2020032616150849800_JWH-D-16-00258C24","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/j.eimc.2014.09.007","article-title":"Nasal carriage of coagulase positive staphylococci in patients of a Primary-Healthcare-Centre: genetic lineages and resistance and virulence genes","volume":"33","author":"Lozano","year":"2015","journal-title":"Enferm. Infecc. Microbiol. Clin."},{"key":"2020032616150849800_JWH-D-16-00258C25","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1007\/s10096-009-0752-2","article-title":"Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers","volume":"28","author":"Monecke","year":"2009","journal-title":"Eur. J. Clin. Microbiol. Dis."},{"key":"2020032616150849800_JWH-D-16-00258C26","doi-asserted-by":"crossref","first-page":"14130","DOI":"10.1073\/pnas.0804178105","article-title":"Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus","volume":"105","author":"N\u00fcbel","year":"2008","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2020032616150849800_JWH-D-16-00258C27","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.vetmic.2011.10.015","article-title":"Clonal diversity of Staphylococcus aureus originating from the small ruminants goats and sheep","volume":"156","author":"Porrero","year":"2012","journal-title":"Vet. Microbiol."},{"key":"2020032616150849800_JWH-D-16-00258C28","doi-asserted-by":"crossref","first-page":"899","DOI":"10.3201\/eid2005.130426","article-title":"Staphylococcus aureus carrying mecC gene in animals and urban wastewater, Spain","volume":"20","author":"Porrero","year":"2014","journal-title":"Infect. Dis."},{"key":"2020032616150849800_JWH-D-16-00258C29","doi-asserted-by":"crossref","first-page":"4090","DOI":"10.1128\/JCM.00820-09","article-title":"Population structure of Staphylococcus aureus strains isolated from Intensive Care Unit patients in the Netherlands over an 11-year period (1996 to 2006)","volume":"47","author":"Rijnders","year":"2009","journal-title":"J. Clin. Microbiol."},{"key":"2020032616150849800_JWH-D-16-00258C30","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.scitotenv.2013.01.032","article-title":"Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review","volume":"447","author":"Rizzo","year":"2013","journal-title":"Sci. Total Environ."},{"key":"2020032616150849800_JWH-D-16-00258C31","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1289\/ehp.1205436","article-title":"Methicillin-resistant Staphylococcus aureus (MRSA) detected at four U.S. wastewater treatment plants","volume":"120","author":"Rosenberg Goldstein","year":"2012","journal-title":"Environ. Health Perspect."},{"key":"2020032616150849800_JWH-D-16-00258C32","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1093\/jac\/45.6.891","article-title":"Prevalence of macrolide-resistance genes in Staphylococcus aureus and Enterococcus faecium isolates from 24 European university hospitals","volume":"45","author":"Schmitz","year":"2000","journal-title":"J. Antimicrob. Chemother."},{"key":"2020032616150849800_JWH-D-16-00258C33","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1111\/j.1574-6941.2003.tb01073.x","article-title":"Detection of antibiotic resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms","volume":"43","author":"Schwartz","year":"2003","journal-title":"FEMS Microbiol. Ecol."},{"key":"2020032616150849800_JWH-D-16-00258C34","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.scitotenv.2007.02.039","article-title":"Application of real-time quantitative PCR for the detection of selected bacterial pathogens during municipal wastewater treatment","volume":"382","author":"Shannon","year":"2007","journal-title":"Sci. Total Environ."},{"key":"2020032616150849800_JWH-D-16-00258C35","first-page":"2178","article-title":"Nosocomial infections and drug susceptibility patterns in methicillin sensitive and methicillin-resistant Staphylococcus aureus","volume":"7","author":"Sharma","year":"2013","journal-title":"J. Clin. Diagn. Res."},{"key":"2020032616150849800_JWH-D-16-00258C36","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1128\/JCM.41.1.456-459.2003","article-title":"Prevalence of agr specificity groups among Staphylococcus aureus strains colonizing children and their guardians","volume":"41","author":"Shopsin","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"2020032616150849800_JWH-D-16-00258C37","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.scitotenv.2015.07.155","article-title":"Faecal pollution source tracking toolbox for identification, evaluation and characterization of faecal contamination in receiving urban surface waters and groundwater","volume":"538","author":"Tran","year":"2015","journal-title":"Sci. Total Environ."},{"key":"2020032616150849800_JWH-D-16-00258C38","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1016\/j.ijmm.2013.02.006","article-title":"The diversity of antimicrobial resistance genes among staphylococci of animal origin","volume":"303","author":"Wendlandt","year":"2013","journal-title":"Int. J. Med. Microbiol."},{"key":"2020032616150849800_JWH-D-16-00258C39","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.tim.2014.10.002","article-title":"Multidrug resistance genes in staphylococci from animals that confer resistance to critically and highly important antimicrobial agents in human medicine","volume":"23","author":"Wendlandt","year":"2015","journal-title":"Trends Microbiol."}],"container-title":["Journal of Water and Health"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/iwaponline.com\/jwh\/article-pdf\/15\/4\/638\/393458\/jwh0150638.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/iwaponline.com\/jwh\/article-pdf\/15\/4\/638\/393458\/jwh0150638.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,3,26]],"date-time":"2020-03-26T23:07:57Z","timestamp":1585264077000},"score":1,"resource":{"primary":{"URL":"https:\/\/iwaponline.com\/jwh\/article\/15\/4\/638\/28591\/Staphylococcus-aureus-isolated-from-wastewater"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,4,5]]},"references-count":39,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2017,4,5]]},"published-print":{"date-parts":[[2017,8,1]]}},"URL":"https:\/\/doi.org\/10.2166\/wh.2017.258","relation":{},"ISSN":["1477-8920","1996-7829"],"issn-type":[{"value":"1477-8920","type":"print"},{"value":"1996-7829","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2017,8,1]]},"published":{"date-parts":[[2017,4,5]]}}}