Emerg Infect DisEmerging Infect. DisEIDEmerging Infectious Diseases1080-60401080-6059Centers for Disease Control and Prevention22469250330967711-141910.3201/eid1804.111419Letters to the EditorLetterMethicillin-Susceptible Staphylococcus aureus ST398, New York and New Jersey, USAMSSA ST398, New York and New JerseyMediavillaJosé R.ChenLiangUhlemannAnne-CatrinHansonBlake M.RosenthalMarnieStanakKathrynKollBrianFriesBettina C.ArmellinoDonnaSchillingMary EllenWeissDonSmithTara C.LowyFranklin D.KreiswirthBarry N.University of Medicine and Dentistry of New Jersey, Newark, New Jersey, USA (J.R. Mediavilla, L. Chen, B.N. Kreiswirth);Columbia University, New York, New York, USA (A.-C. Uhlemann, F.D. Lowy);University of Iowa, Iowa City, Iowa, USA (B.M. Hanson, T.C. Smith);Jersey Shore University Medical Center, Neptune, New Jersey, USA (M. Rosenthal);Beth Israel Medical Center, New York (K. Stanak, B. Koll);Albert Einstein College of Medicine, Bronx, New York, USA (B.C. Fries);North Shore University Hospital, Manhasset, New York, USA (D. Armellino, M.E. Schilling);New York City Department of Health and Mental Hygiene, New York (D. Weiss)Address for correspondence: Barry N. Kreiswirth, Public Health Research Institute Tuberculosis Center, University of Medicine and Dentistry of New Jersey, 225 Warren St, ICPH W210M, Newark, NJ 07103, USA; email: kreiswba@umdnj.edu42012184700702Keywords: Staphylococcus aureusMSSAST398CC398livestock-associatedhumaninfectionbacteriaNew YorkNew JerseystaphylococciUnited States

To the Editor: Clinical infections with livestock-associated Staphylococcus aureus sequence type (ST) 398 have been reported in Europe, Canada, and the People’s Republic of China (1), as well as the Caribbean (2,3), and Colombia (4). Most reports describe infection with methicillin-resistant S. aureus; relatively few describe infection with methicillin-susceptible S. aureus (MSSA). In the United States, colonization of healthy adults by ST398 has been reported in Iowa (5) and in New York, New York (2); MSSA infections have been anecdotally reported in St. Louis, Missouri (6), and The Bronx, New York (7). We describe 8 infections with MSSA ST398 in the New York City area during a 7-year period (2004–2010). Five infections with a related ST (ST291) from clonal complex (CC) 398 also were identified. These findings highlight the emergence of clinical infections with 2 distinct CC398 sequence types in the New York City area.

Retrospective typing of 4,167 clinical S. aureus isolates from various studies involving inpatients and outpatients in the New York City area identified 13 mecA-negative isolates with CC398-associated spa types (Table). Nine isolates were obtained from cultures of outpatients with skin and soft tissue infections; samples were submitted by physicians in the community. One isolate was associated with recurring skin and soft tissue infections in multiple body sites (BK21466); another was associated with genital infection (BK21732). Of the 4 ST398 isolates derived from bloodstream infections in hospitalized patients, 3 were recovered from intravenous drug users, 1 of whom died 1 day after admission for variceal bleeding (BK26722). Unlike the multidrug-resistant ST398 MSSA recently described in Colombia (4), most isolates in this study were susceptible to all antimicrobial drugs tested except penicillin, although several strains exhibited resistance to clindamycin and erythromycin. One isolate (BK23527) was submitted as oxacillin resistant (MIC ≥4 μg/mL) but lacked the mecA gene, which suggested that another mechanism was contributing to the resistance phenotype.

Characteristics of <italic>Staphylococcus aureus</italic> clonal complex 398 isolates, New York and New Jersey, USA, 2004–2010*
Isolate†YearGeographic location‡Submitting institution§Isolate sourceAntimicrobial resistancePFGE patternspa typespa repeatsRidom typeST
BK136842004Monmouth County, NJLaboratory AWoundPEN539XKAOAOBQOt034398
BK185052006ManhattanLaboratory AWoundA1109XKAOAOBOt571398
BK214662007Staten IslandLaboratory AArm, face, leg, buttocksA2109XKAOAOBOt571398
BK217322007ManhattanLaboratory AGenitalPEN, CLI, ERYA3109XKAOAOBOt571398
BK270372007The BronxHospital ABlood, lung abscessPEN, CLI, ERYA4109XKAOAOBOt571398
BK235272008ManhattanHospital BBlood, buttocksPEN, ERY, OXA109XKAOAOBOt571398
BK267222009ManhattanHospital BBloodCLI, ERYA1109XKAOAOBOt571398
BK312742010Nassau County, NYHospital CBlood, sternumPEN, CLI, ERYA11376XKAOBOt1451398
BK137712004Somerset County, NJLaboratory AWoundPEN, ERYB4716XKBBMt2993291
BK134512004Union County, NJLaboratory AWoundPENB2718XKBQBMMt1149291
BK193822006Staten IslandLaboratory ARight earPENB1865XKBQBBMt2313291
BK217462007ManhattanLaboratory ATorsoPEN, ERYB1208XKBQBBMMt937291
BK221832007ManhattanLaboratory AAxillaPENB3208XKBQBBMMt937291

*Antimicrobial drug susceptibilities were obtained from submitting institutions (unavailable for BK18505 and BK21466). PFGE was performed by using Cfr9I, with patterns assigned on the basis of 80% similarity cutoffs (BioNumerics version 6.5, Applied Maths, Austin, TX, USA); BK13684 and BK23527 were unavailable for PFGE analysis. spa typing was performed by using eGenomics software (www.egenomics.com), and Ridom spa types were assigned by using the SpaServer Web site (www.spaserver.ridom.de). Multilocus sequence typing was performed as described (http://saureus.mlst.net). PFGE, pulsed-field gel electrophoresis; spa, staphylococcal protein A; ST, sequence type; wound, skin and soft-tissue infections from unspecified body sites; PEN, penicillin; CLI, clindamycin; ERY, erythromycin; OXA, oxacillin (resistance >4 μg/mL was reported for BK23527, but mecA was not detected by real-time PCR).
†BK27037 has been described (7).
‡Manhattan, Staten Island, and the Bronx are boroughs of New York, New York.
§Laboratory A is a large outpatient commercial laboratory serving the metropolitan New York, New York, area.

Multilocus sequence typing confirmed 8 isolates as ST398 (3–35–19–2–20–26–39); 5 isolates were assigned to ST291 (3–37–19–2–20–26–32), a double-locus variant of ST398 (Figure A1, panel A). Most of the ST398 strains were spa type 109 (t571), described in MSSA carriage isolates from New York City (2) and MSSA infections from China (1), France (8), Martinique (3), the Dominican Republic (2,3), and Colombia (4). BURP (based upon repeat pattern) analysis clustered all of the spa types into spa-CC t571 (Figure A1, panel B); ST398 isolates clustered with spa type 109 (t571), whereas ST291 isolates clustered with spa type 865 (t2313). Pulsed-field gel electrophoresis was also performed on the 11 available isolates. Although the ST291 isolates were sensitive to digestion with SmaI, pulsed-field gel electrophoresis was performed with Cfr9I to compare all isolates simultaneously. As expected, the ST398 and ST291 isolates clustered separately (data not shown); 4 distinct patterns were observed within each cluster (Table). Only the ST398 isolates were positive for a CC398 lineage-specific PCR that targets the unique restriction-modification system sau1-hsdS1 (9), further highlighting the differences between ST291 and ST398. None of the isolates harbored the genes coding for Panton-Valentine leukocidin.

Because of the retrospective nature of the findings, epidemiologic information for each isolate was limited. One patient (BK19382) reported travel to the Dominican Republic; Caribbean nationality was reported for BK27037 (Puerto Rico) and BK31274 (Trinidad). The cases described here occurred in urban and suburban settings, reflecting the likelihood that exposure to livestock was relatively low; however, travel history was unknown for most of the patients. Previous reports have linked ST398 transmission to other reservoirs, including companion animals, live animal food markets, and commercial meat products (1,2). However, data from a recent genome sequencing study suggest that MSSA ST398 is human in origin (10); other evidence suggests that certain lineages, particularly spa type 109 (t571), might circulate at low levels in humans in the absence of livestock exposure (8).

Our findings seem to support the hypothesis of low-level ST398 MSSA prevalence, and further surveillance might uncover additional cases of colonization or infection with ST398- and ST291-related strains in the New York City area. For example, active surveillance cultures performed at one of the 3 hospitals during January–March 2009 detected 7 additional ST398 and 3 additional ST291 isolates among 260 MSSA carriage strains (data not shown). In addition to the intrinsic virulence exhibited by ST398 MSSA in previous studies, the potential to acquire resistance to multiple classes of antimicrobial drugs (1,4,10), as well as virulence factors such as Panton-Valentine leukocidin (8), warrants continued surveillance in light of recent ST398 methicillin-resistant S. aureus outbreaks in health care settings (1).

Suggested citation for this article: Mediavilla JR, Chen L, Uhlemann A-C, Hanson BM, Rosenthal M, Stanak K et al. Methicillin-susceptible Staphylococcus aureus ST398, New York and New Jersey, USA [letter]. Emerg Infect Dis [serial on the Internet]. 2012 Apr [date cited]. http://dx.doi.org/10.3201/eid1804.111419

Acknowledgments

We thank Bruce F. Farber for administrative support and clinical guidance and John Gattringer, Nancy Musa, and Michael Henry for gathering data related to this project.

This work was partially funded by the New York State Department of Health Hospital-Acquired Infection Reporting Program (D.A., M.E.S.) and Infection Prevention Project Program (K.S., B.K.) and by a grant from the New York Community Trust (B.N.K.).

A) Schematic representation of Staphylococcus aureus clonal complex (CC) 398, generated by eBURST version 3 from the S. aureus multilocus sequence typing database (http://saureus.mlst.net) as of September 2011. Subgroup founders sequence type (ST) 398 (3–35–19–2–20–26–39) and ST291 (3–37–19–2–20–26–32) are double locus variants, despite the depiction of intervening STs ST804 (3–35–19–2–20–26–2) and ST813 (3–37–19–2–20–26–2). Subgroup founders are denoted in larger font. B) spa clonal complex (spa-CC) t571, generated by using the integrated BURP (based upon repeat patterns) algorithm in Ridom StaphType software, version 1.5 (www.ridom.de/staphtype). ST398-associated spa types (t034, t571, t1451) and ST291-associated spa types (t937, t1149, t2313, t2993) described in the article cluster separately as in panel A. Subgroup founders are denoted in larger font.

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