Emerging Infectious Diseases Volume 18 Issue 10

2012·4.6 MB·English

by  CDC

Peer-Reviewed Journal Tracking and Analyzing Disease Trends pages 1557–1716
EDITOR-IN-CHIEF
D. Peter Drotman
Managing Senior Editor EDITORIAL BOARD
Polyxeni Potter, Atlanta, Georgia, USA
Dennis Alexander, Addlestone, Surrey, UK
Associate Editors Timothy Barrett, Atlanta, Georgia, USA
Paul Arguin, Atlanta, Georgia, USA Barry J. Beaty, Ft. Collins, Colorado, USA
Charles Ben Beard, Ft. Collins, Colorado, USA Martin J. Blaser, New York, New York, USA
Ermias Belay, Atlanta, Georgia, USA Christopher Braden, Atlanta, Georgia, USA
David Bell, Atlanta, Georgia, USA Arturo Casadevall, New York, New York, USA
Sharon Bloom, Atlanta, GA, USA Kenneth C. Castro, Atlanta, Georgia, USA
Mary Brandt, Atlanta, Georgia, USA Louisa Chapman, Atlanta, Georgia, USA
Corrie Brown, Athens, Georgia, USA Thomas Cleary, Houston, Texas, USA
Charles H. Calisher, Ft. Collins, Colorado, USA Vincent Deubel, Shanghai, China
Michel Drancourt, Marseille, France Ed Eitzen, Washington, DC, USA
Paul V. Effl er, Perth, Australia Daniel Feikin, Baltimore, Maryland, USA
David Freedman, Birmingham, Alabama, USA Anthony Fiore, Atlanta, Georgia, USA
Peter Gerner-Smidt, Atlanta, Georgia, USA Kathleen Gensheimer, Cambridge, Massachusetts, USA
Stephen Hadler, Atlanta, Georgia, USA Duane J. Gubler, Singapore
Nina Marano, Atlanta, Georgia, USA Richard L. Guerrant, Charlottesville, Virginia, USA
Martin I. Meltzer, Atlanta, Georgia, USA Scott Halstead, Arlington, Virginia, USA
David Morens, Bethesda, Maryland, USA David L. Heymann, London, UK
J. Glenn Morris, Gainesville, Florida, USA Charles King, Cleveland, Ohio, USA
Patrice Nordmann, Paris, France Keith Klugman, Atlanta, Georgia, USA
Tanja Popovic, Atlanta, Georgia, USA Takeshi Kurata, Tokyo, Japan
Didier Raoult, Marseille, France S.K. Lam, Kuala Lumpur, Malaysia
Pierre Rollin, Atlanta, Georgia, USA Stuart Levy, Boston, Massachusetts, USA
Ronald M. Rosenberg, Fort Collins, Colorado, USA John S. MacKenzie, Perth, Australia
Dixie E. Snider, Atlanta, Georgia, USA Marian McDonald, Atlanta, Georgia, USA
Frank Sorvillo, Los Angeles, California, USA John E. McGowan, Jr., Atlanta, Georgia, USA
David Walker, Galveston, Texas, USA Tom Marrie, Halifax, Nova Scotia, Canada
J. Todd Weber, Atlanta, Georgia, USA Philip P. Mortimer, London, UK
Fred A. Murphy, Galveston, Texas, USA
Founding Editor
Barbara E. Murray, Houston, Texas, USA
Joseph E. McDade, Rome, Georgia, USA
P. Keith Murray, Geelong, Australia
Senior Associate Editor, Emeritus Stephen M. Ostroff, Harrisburg, Pennsylvania, USA
Brian W.J. Mahy, Bury St. Edmunds, Suffolk, UK Richard Platt, Boston, Massachusetts, USA
Copy Editors Claudia Chesley, Karen Foster, Thomas Gryczan, Gabriel Rabinovich, Buenos Aires, Argentina
Jean Michaels Jones, Carol Snarey, P. Lynne Stockton Mario Raviglione, Geneva, Switzerland
David Relman, Palo Alto, California, USA
Production Carrie Huntington, Ann Jordan, Shannon O’Connor,
Connie Schmaljohn, Frederick, Maryland, USA
Reginald Tucker
Tom Schwan, Hamilton, Montana, USA
Editorial Assistant Christina Dzikowski Ira Schwartz, Valhalla, New York, USA
Tom Shinnick, Atlanta, Georgia, USA
Social Media/Communications Sarah Logan Gregory
Bonnie Smoak, Bethesda, Maryland, USA
Emerging Infectious Diseases is published monthly by the Centers for Disease Rosemary Soave, New York, New York, USA
Control and Prevention, 1600 Clifton Road, Mailstop D61, Atlanta, GA 30333, P. Frederick Sparling, Chapel Hill, North Carolina, USA
USA. Telephone [phone], fax [phone], email [email protected]. Robert Swanepoel, Pretoria, South Africa
The opinions expressed by authors contributing to this journal do not neces- Phillip Tarr, St. Louis, Missouri, USA
sarily refl ect the opinions of the Centers for Disease Control and Prevention or Timothy Tucker, Cape Town, South Africa
the institutions with which the authors are affi liated. Elaine Tuomanen, Memphis, Tennessee, USA
All material published in Emerging Infectious Diseases is in the public do-
John Ward, Atlanta, Georgia, USA
main and may be used and reprinted without special permission; proper citation,
Mary E. Wilson, Cambridge, Massachusetts, USA
however, is required.
Use of trade names is for identifi cation only and does not imply endorsement
by the Public Health Service or by the U.S. Department of Health and Human ∞ Emerging Infectious Diseases is printed on acid-free paper that meets the requirements
of ANSI/NISO 239.48-1992 (Permanence of Paper)
Services.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 10, October 2012
October 2012
On the Cover WU and KI Polyomaviruses in
Mori Sosen (1747–1821) Respiratory Samples from
Monkey Performing the Sanbasō Dance Allogeneic Hematopoietic Cell
(Dated 1800, the fi rst day of the Monkey Year) Transplant Recipients ......................1580
Scroll painting, ink on paper
J. Kuypers et al.
(49.5 cm x 115.6 cm)
Pacifi c Asia Museum, Pasadena, California, USA, Routine testing for these viruses in immuno-
Gift of Mr. and Mrs. Bruce Ross compromised patients is not recommended.
www.pacifi casiamuseum.org
Wild Birds and Urban Ecology
About the Cover p. 1711
of Ticks and Tick-borne
Pathogens, Chicago, Illinois,
Research 2005–2010..........................................1589
S.A. Hamer et al.
The rare introduction but successful
establishment of ticks and pathogens poses a
Methicillin-Resistant signifi cant health risk.
Staphylococcus aureus
Sequence Type 239-III, Spread of Infl uenza Virus A (H5N1)
Ohio, 2007–2009 ...............1557 Clade 2.3.2.1 to Bulgaria in
S.-H. Wang et al. Common Buzzards ...........................1596
Identifi cation of virulent strains emphasizes the A. Marinova-Petkova et al.
need for molecular surveillance.
Detection of this highly pathogenic clade in
Europe poses a health threat to both humans
p. 1578
and poultry.
Epidemiology of Dengue Outbreaks in High-Income
Foodborne Norovirus Area, Kaohsiung City, Taiwan,
Outbreaks, United States, 2003–2009..........................................1603
2001–2008 .........................1566 C.-H. Lin et al.
A.J. Hall et al. Cases are distributed in a clustered pattern, and
Interventions should focus on commercial food p. 1623 elderly persons have the highest risk for illness
and death.
handlers and production of commodities eaten
raw.
Nontuberculous Mycobacteria
in Household Plumbing as
Constant Transmission
Possible Cause of Chronic
Properties of Variant
Rhinosinusitis ...................................1612
Creutzfeldt-Jakob Disease in
W.S. Tichenor et al.
5 Countries ........................................1574
Patients with treatment-resistant rhinosinusitis
A.B. Diack et al.
should have cultures performed for NTM; also,
Current diagnostic criteria should be suffi cient sinuses should not be irrigated with tap water.
to detect new cases.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 10, October 2012 i
Autochthonous and Dormant
Cryptococcus gattii Infections
in Europe ...........................................1618 October 2012
F. Hagen et al.
1662 Visceral Leishmaniasis in
Dormant infections can be reactivated many
Rural Bihar, India
years after having been acquired on another
E. Hasker et al.
continent.
1665 Circulation of Infl uenza A(H1N1)
Dispatches
pdm09 Virus in Pigs, Réunion
Island
1625 Echinococcus multilocularis in
E. Cardinale et al.
Urban Coyotes, Alberta, Canada
S. Catalano et al.
1669 Powassan Virus Encephalitis,
Minnesota
1629 Orthobunyavirus Antibodies in
p. 1648 J. Birge and S. Sonnesyn
Humans, Yucatan Peninsula,
Mexico
B.J. Blitvich et al. 1672 Infl uenza Virus Infection in
Nonhuman Primates
E.A. Karlsson et al.
1633 Tetanus as Cause of Mass Die-off
of Captive Japanese Macaques,
Japan, 2008 1676 Human Polyomaviruses
T. Nakano et al. in Children Undergoing
Transplantation, United States,
2008–2010
1636 Human Infection with Candidatus
E.A. Siebrasse et al.
Neoehrlichia mikurensis, China
H. Li et al.
1680 Preventing Maritime Transfer of
Toxigenic Vibrio cholerae
1640 Anthroponotic Enteric Parasites
N.J. Cohen et al.
in Monkeys in Public Park, China
J. Ye et al.
Another Dimension
1644 Schmallenberg Virus as Possible p. 1669
Ancestor of Shamonda Virus 1684 A Natural History of Infective
K.V. Goller et al. Endocarditis, Preceded by
Decompensated Chronic Liver
Disease and Severe Community-
1647 Monkey Bites among US Military
acquired Pneumonia
Members, Afghanistan, 2011
N.L. Merridew
L.E. Mease and K.A. Baker
1650 Human Parvovirus 4 in Nasal and Letters
Fecal Specimens from Children,
Ghana 1686 Trypanososma brucei
J.F. Drexler et al. rhodesiense Sleeping Sickness,
Uganda
1654 Hepatitis E Virus Seroprevalence
among Adults, Germany 1687 Rickettsia felis in Aedes
M.S. Faber et al. albopictus Mosquitoes, Libreville,
Gabon
1658 Scarlet Fever Epidemic, Hong
Kong, 2011 1689 Bartonella spp. Infection Rate and
E.Y.Y. Luk et al. B. grahamii in Ticks
ii Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 10, October 2012
1704 Duffy Phenotype and
Plasmodium vivax Infections in
October 2012 Humans and Apes, Africa
1690 Human Parvovirus 4 Viremia in
1705 Rickettsia parkeri and
Young Children, Ghana
Candidatus Rickettsia andeanae
in Gulf Coast Ticks, Mississippi
1692 Multidrug-Resistant Salmonella
enterica, Democratic Republic of
1707 Attributing Cause of Death
the Congo
for Patients with Clostridium
diffi cile Infection
1694 Co-Circulation and Persistence
of Genetically Distinct Saffold
1708 Characterization of
Viruses, Denmark
Mycobacterium orygis
p. 1673
1696 Pathogenic Leptospira spp. in
1709 Epsilonproteobacteria in
Bats, Madagascar and Union of
Humans, New Zealand
the Comoros
p. 1703
About the Cover
1698 West Nile Virus
Meningoencephalitis Imported
1711 Human minus Three Pieces of
into Germany
Hair
1700 Scarlet Fever Outbreak,
Etymologia
Hong Kong, 2011
1635 Tetanus
1702 Hand, Foot, and Mouth Disease
Caused by Coxsackievirus A6
Conference Summaries/
Reports Online Only
wwwnc.cdc.gov/eid/articles/online-reports.htm
Manuscripts submitted for online publication may
include illustrations and relevant links.
More information on online only
requirements at
wwwnc.cdc.gov/eid/pages/author-resource-center.htm
Submit manuscripts at
wwwnc.cdc.gov/eid/pages/submit-manuscript.htm
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 10, October 2012 iii
iv Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 10, Octoer 2012
Methicillin-Resistant
Staphylococcus aureus Sequence
Type 239-III, Ohio, USA, 2007–20091
Shu-Hua Wang, Yosef Khan, Lisa Hines, José R. Mediavilla, Liangfen Zhang, Liang Chen,
Armando Hoet, Tammy Bannerman, Preeti Pancholi, D. Ashley Robinson, Barry N. Kreiswirth,
and Kurt B. Stevenson, for the Prevention Epicenter Program of the Centers for Disease Control
and Prevention
Medscape, LLC is pleased to provide online continuing medical education (CME) for this journal article, allowing clinicians the
opportunity to earn CME credit.
This activity has been planned and implemented in accordance with the Essential Areas and policies of the Accreditation
Council for Continuing Medical Education through the joint sponsorship of Medscape, LLC and Emerging Infectious Diseases.
Medscape, LLC is accredited by the ACCME to provide continuing medical education for physicians.
Medscape, LLC designates this Journal-based CME activity for a maximum of 1 AMA PRA Category 1 Credit(s)TM. Physicians
should claim only the credit commensurate with the extent of their participation in the activity.
All other clinicians completing this activity will be issued a certificate of participation. To participate in this journal CME activity:
(1) review the learning objectives and author disclosures; (2) study the education content; (3) take the post-test with a 70% minimum
passing score and complete the evaluation at www.medscape.org/journal/eid; (4) view/print certificate.
Release date: September 20, 2012; Expiration date: September 20, 2013
Learning Objectives
Upon completion of this activity, participants will be able to:
• Distinguish the most common strains of methicillin-resistant Staphylococcus aureus (MRSA) in the United States
• Assess the clinical characteristics of infection with MRSA ST239-III
• Analyze the treatment and prognosis of MRSA ST239-III infection
• Evaluate molecular characteristics of MRSA ST239-III.
CME Editor
Thomas J. Gryczan, MS, Technical Writer/Editor, Emerging Infectious Diseases. Disclosure: Thomas J. Gryczan, MS, has
disclosed no relevant financial relationships.
CME Author
Charles P. Vega, MD, Health Sciences Clinical Professor; Residency Director, Department of Family Medicine, University of
California, Irvine. Disclosure: Charles P. Vega, MD, has disclosed no relevant financial relationships.
Authors
Disclosures:Shu-Hua Wang, MD, MPH; Yosef Khan, MBBS, PhD; Jose R. Mediavilla, MBS, MPH; Liangfen Zhang, MD,
PhD; Liang Chen, PhD; Armando Hoet, PhD; Tammy Bannerman; D. Ashley Robinson, PhD; Barry N. Kreiswirth, PhD; and
Kurt B. Stevenson, MD, MPH, have disclosed no relevant financial relationships. Lisa Hines, RN, CIC, has disclosed the following
relevant financial relationships: owns stock, stock options, or bonds from Kimberly Clark Corp., General Electric Co., Medtronic Inc.,
Stryker Corp. TEVA Pharmaceutical Industries. Preeti Pancholi, PhD, has disclosed the following relevant financial relationships:
served as an advisor or consultant for Abbott; served as a speaker or a member of a speakers bureau for Abbott, Nanosphere;
received grants for clinical research from Cepheid, Abbott, Quidel, QIAGEN, Nanosphere.
Author affi liations: The Ohio State University Wexner Medical Methicillin-resistant Staphylococcus aureus (MRSA) is
Center, Columbus, Ohio, USA (S.H. Wang, Y. Khan, L. Hines, A. a human pathogen that has diverse molecular heterogeneity.
Hoet, P. Pancholi, K.B. Stevenson); University of Medicine and Most MRSA strains in the United States are pulsed-fi eld gel
electrophoresis USA100 sequence type (ST) 5 and USA300
Dentistry of New Jersey, Newark, New Jersey, USA (J.R. Mediavilla,
ST8. Infections with MRSA ST239-III are common and
L. Chen, B.N. Kreiswirth); University of Mississippi Medical Center,
found during health care–associated outbreaks. However,
Jackson, Mississippi, USA (L. Zhang, D.A. Robinson); and The
this strain has been rarely reported in the United States.
Ohio Department of Health Laboratories, Reynoldsburg, Ohio, USA
1Presented in part at the 48th Annual Meeting of the Infectious
(T. Bannerman)
Diseases Society of America, Vancouver, British Columbia,
DOI: http://dx.doi.org/10.3201/eid1810.120468 Canada, October 21–24, 2010.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 10, October 2012 1557
RESEARCH
As part of a study supported by the Prevention Epicenter Program study evaluating the transmission of MRSA between
Program of the Centers for Disease Control and Prevention hospitals in Ohio, USA, molecular analysis was performed
(Atlanta, GA, USA), which evaluated transmission of MRSA on a group of clinical MRSA isolates collected from The
among hospitals in Ohio, molecular typing identifi ed 78 Ohio State Health Network (OSHN). The OSHN consists of
(6%) of 1,286 patients with MRSA ST239-III infections.
The Ohio State University (OSU) Wexner Medical Center
Ninety-fi ve percent (74/78) of these infections were health
(WMC), which is a tertiary care medical center, and 7 smaller
care associated, and 65% (51/78) of patients had histories
community hospitals located 30–120 miles from OSU. All
of invasive device use. The crude case-fatality rate was
MRSA specimens from community hospitals and selected
22% (17/78). Identifi cation of these strains, which belong to
OSU MRSA blood isolates and isolates from patients
a virulent clonal group, emphasizes the need for molecular
surveillance. residing in the catchment areas of the outreach hospitals
were prospectively collected during March 2009–February
2010 for genotyping by using a repetitive element PCR (rep-
Staphylococcus aureus is a major human pathogen that
PCR). Among archived MRSA isolates from OSUWMC
possesses multiple toxins and virulence mechanisms
from January 2007 through February 2009, only a selection
(1). Antimicrobial drug resistance in S. aureus has added to
of isolates was chosen for genotyping (not a randomized
the complexity of treating serious infections caused by this
sampling). The total number of isolates and the total number
bacteria, and methicillin-resistant S. aureus (MRSA) appears
of ST239 from each time period was collected.
to have greater virulence than methicillin-susceptible
strains (2,3). Most MRSA strains in the United States are
Data Collection
pulsed-fi eld gel electrophoresis (PFGE) types USA100 and
We performed medical record reviews for 1,286
USA300, corresponding to multilocus sequence typing
patients. Patient demographic characteristics (presence of
(MLST) ST5 and ST8, respectively (4). MRSA belonging
health care–related risk factors during the preceding 12
to MLST ST239 and harboring staphylococcal cassette
months, presence of an invasive device during the previous
chromosome mec (SCCmec) type III (MRSA ST239-
7 days, and concurrent conditions) were collected. Patient-
III) are associated with infections in health care settings,
level data, including addresses for geocoding, were entered
outbreaks, increased resistance to antimicrobial drugs, and
into a secure database within the OSUWMC Information
capacity for invasive disease (5–7).
Warehouse.
MRSA ST239-III has a history of successful
dissemination in many regions, leading to a diverse array
Classifi cation of MRSA Infections
of regionally prevalent clones. These clones include the
All MRSA cases were classifi ed into 3 categories on
Brazilian; British Epidemic 1, 4, 7, 9, and 11; Canadian
the basis of accepted epidemiologic defi nitions (11). The
Epidemic 3/Punjab; Czech; Eastern Australian 2 and 3;
fi rst category was health care–associated, defi ned as a
Georgian; Hungarian; Lublin; Nanjing/Taipei (ST241);
culture obtained >48 hours after admission. The second
Portuguese; and Vienna clones (8,9). Although it is
category was health care–associated community onset,
common worldwide, MRSA ST239-III has not played
defi ned as a culture obtained <48 hours after admission
any predominant role in the United States; infections with
with identifi ed health care–associated risk factors. The
MRSA ST239-III have been rarely reported in the United
third category was community-associated, defi ned as a
States since the 1990s (9–13). Recently, only 2 reports
culture obtained <48 hours after admission without health
of this strain in the United States involving sporadic
care–associated risk factors. Health care–associated risk
nasal colonization and bloodstream infections have been
factors comprised presence of an invasive device, history of
published (13,14).
MRSA infection or colonization, surgery, hospitalization,
In this study, we describe clinical epidemiologic
dialysis, or residence in a long-term care facility in the 12
characteristics and molecular analysis of clinical infections
months preceding the culture.
with MRSA ST239-III in the midwestern United States.
Outcomes for MRSA infection were categorized
Identifi cation of a strain from such a virulent clonal group
as cure (complete resolution after antimicrobial drug
in the United States with wide dissemination in other parts
treatment); failure (persistence of infection and change in
of the world represents a potential public health concern.
antimicrobial drug regimen); relapse (resolution of infection
after complete treatment with subsequent development of
Methods
new symptoms); recurrent (redevelopment of MRSA at
same or other site >2 weeks after completion of treatment
Sampling Method
for initial MRSA infection); indeterminate (unknown
As part of Centers for Disease Control and Prevention
outcome); and death (death <30 days after diagnosis of
(CDC) (Atlanta, GA, USA)–sponsored Prevention Epicenter
MRSA infection because of any cause or during the same
1558 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 10, October 2012
MRSA Sequence Type 239-III, Ohio, USA, 2007–2009
hospitalization). Destination after hospital discharge, such used because we were not analyzing for an outbreak (17).
as home or skilled nursing facility, was also noted. Thus, interpretations of possibly or probably related PFGE
subtypes between strains obtained by PFGE band patterns
Drug Susceptibility Testing were not made. Each PFGE band difference was classifi ed
The respective OSHN Clinical Microbiology as a unique PFGE pattern.
Laboratories initially identifi ed all MRSA isolates by using
standard microbiological methods. Antimicrobial drug spa Typing
susceptibility testing was performed at each institution, spa typing (18) was performed on all MRSA isolates
and results were interpreted according to Clinical and by using eGenomics software (www.egenomics.com)
Laboratory Standards Institute break point guidelines (15). as described (19); Ridom spa types were subsequently
At OSUWMC, antimicrobial drug susceptibility testing assigned by using the SpaServer website (www.spaserver.
was performed by using the automated Micro-Scan method ridom.de).
(Siemens Diagnostics, Sacramento, CA, USA), and only
constitutive clindamycin testing was performed. Linezolid SCCmec Typing
MIC >4 mg/L were confi rmed by using the Etest method SCCmec typing was performed on all MRSA isolates
(bioMérieux, Marcy l’Etoile, France). by using a described multiplex real-time PCR (20). This
PCR is specifi c for 2 essential gene complexes (ccr and
Genotyping mec) found in all SCCmec elements.
The MRSA ST239 III isolates were genotyped initially
by using rep-PCR, followed by PFGE, staphylococcal dru Typing
protein A sequencing (spa typing), SCCmec typing, and MRSA isolates were also characterized by sequencing
mec-associated direct repeat unit (dru) typing. Selected the hypervariable dru repeat region within the SCCmec
isolates were also characterized by MLST and single- element (21) and using DruID software (9). New dru types
nucleotide polymorphism (SNP) typing. Detection of genes were submitted to www.dru-typing.org.
encoding Panton–Valentine leukocidin (PVL), toxic shock
syndrome toxin (TSST), arginine catabolic mobile element MLST and PVL, TSST, ACME, and Mupirocin
(ACME), and high-level mupirocin resistance (mupA) was Resistance
also performed. Brief descriptions of each testing method MLST was performed on representative isolates as
are outlined below. described (22) by using the MLST database (http://saureus.
mlst.net). PCR-based detection of PVL (23), TSST (24),
rep-PCR ACME (25), and mupA (26) was performed on all isolates
The DiversiLab System (bioMérieux, Durham, as described.
NC, USA) was used for rep-PCR analysis according to
described methods (16). Isolates belonging to designated SNP Typing
rep-PCR clusters shared >95% similarity. In addition, A panel of 43 SNPs for describing the global population
comparison of matching patterns in the DiversiLab System structure of MRSA ST239-III (9) was used to identify the
library was initially used to infer the PFGE and SCCmec haplotypes of 22 isolates. These SNPs were typed by using
types, which were later validated by using appropriate Golden-Gate Genotyping Assay (Illumina, San Diego, CA,
testing methods. The numeric classifi cation system used USA) and conventional Sanger sequencing.
for rep-PCR analysis is unique to OSUWMC.
Statistical Analysis
PFGE All patient demographic, clinical, and molecular typing
The PulseNet protocol for molecular subtyping of data were aggregated in tabular format, and descriptive
S. aureus was followed. Salmonella enterica serotype statistics were generated by using SAS version 9.2 (SAS
Braenderup DNA was digested with XbaI (Roche, Institute Inc., Cary NC, USA), for demographic and risk
Indianapolis, IN, USA) and used as the normalization factor history. A signifi cant difference between ST239 and
standard for gel analysis. S. aureus chromosomal DNA was other strains (US300, US100, and all other strains) was
digested with SmaI (Roche). Fragments were separated in examined by using χ2 tests for categorical variables and
a clamped homogenous electric fi eld mapper unit (Bio-Rad t-tests for continuous variables. An α level of 0.5 was used.
Laboratories, Hercules, CA, USA). Fingerprint images
were analyzed by using Bionumerics software version Human Subjects Protection
4.61 (Applied Maths NV, Sint-Martens-Latem, Belgium). We obtained approval for this study from the OSU
The traditional classifi cation of PFGE subtypes was not Offi ce of Responsible Research Practices’ Biomedical
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 10, October 2012 1559
RESEARCH
Institutional Review Board. The OSU Information For linezolid, 69 (97%) of 71 isolates were susceptible
Warehouse has established honest broker status with the and 2 blood isolates with MICs >4 mg/L were classifi ed as
OSU Institutional Review Board, enabling storage of uninterpretable.
fully identifi able data and presentation of patient data to
investigators in a coded format that maintains patient Molecular Typing of MRSA ST239-III Isolates
confi dentiality. Eight rep-PCR patterns (6, 19, 22, 42, 53, 78, 79, and
97) were detected among MRSA ST239-III isolates, and 39
Results (50%) isolates had rep-PCR pattern 6. Similarly, isolates
were distributed among 9 PFGE patterns (A, B, C, D, E,
Patient Characteristics F, G, H, and I), and 58 (74%) had PFGE pattern A. The
Of 1,286 clinical MRSA isolates, 78 (6%) were rep-PCR and PFGE patterns are shown in Figure 1. PFGE
identifi ed as MRSA ST239-III; 71 (91%) were obtained pattern F is <80% similar with other PFGE subtypes in
from OSU and 7 (9%) from community hospitals. the dendrogram and was identifi ed as an unknown PFGE
Seven (2%) of 397 isolates were obtained from outreach type by the CDC database. However, molecular testing
community hospitals, 37 (6%) of 613 from OSUWMC, and confi rmed it to be MRSA ST239-III: MLST 239, SCCmec
34 (12%) of 276 from OSUWMC archives. type III, spa type 3(t037), dru type dt15b, and SNP
These strains were fi rst recognized by rep-PCR as haplotype H9.
possible SCCmecA type III isolates from the DiversiLab Four spa types, including eGenomics spa types 3
System library with imputed Brazilian PFGE types. (Ridom t037), 314 (t363), 121 (t421), and 1256 (t631)
Additional molecular typing identifi ed MRSA ST239-III in were identifi ed, and 74 (95%) isolates were classifi ed as
a clade different from that containing the Brazilian strains. spa type 3 (t037). In contrast, isolates were grouped into
Demographics and clinical characteristics of 78 13 dru types (dt2c, dt6n, dt9g, dt12i, dt13k, dt14 g, dt15b,
patients infected with MRSA ST239-III are shown in the dt15h, dt15i, dt15j, dt15k, dt16a, and dt23a), and 60 (77%)
Table. Among patients with MRSA ST239-III infections, isolates were classifi ed as dt15b. MLST typing of selected
46 (59%) were male, 65 (83%) were white, 31 (40%) representative isolates confi rmed 13 to be MRSA ST239-
disabled, and 29 (37%) were retired. Seventy-four (95%) III (2-3-1-1-4-4-3), 3 as ST1801 (2-3-1-1-4-19-3), and 1
had health care–associated isolates and 51 (65%) had as ST2017 (2-3-1-1-4-19-227). ST1801 is a single-locus
histories of use of invasive devices within the previous variant of MRSA ST239-III, and ST2017 is a novel single-
7 days. Distribution of specimen types include 37 (47%) locus variant of ST1801 and a double-locus variant of
bloodstream infections (BSIs), 19 (24%) lower respiratory MRSA ST239. All were SCCmec type III, and the ccrC
tract infections (LRTIs), 11 (14%) skin and soft tissue locus was not detected. The genes that encode PVL, TSST,
infections, and 11 (14%) other infections. Seventeen (22%) ACME, or high-level mupirocin resistance were not found
patients died, and 18 (23%) patients had treatment failures, in any isolates.
recurring infections, or relapses. Only 32% of the patients A total of 33 unique genotypic combinations from 78
were discharged home. patients infected with MRSA ST239-III were represented
Comparison of clinical characteristics of MRSA among isolates with complete SCCmec, rep-PCR, PFGE,
ST239-III with those of PFGE types USA100 and USA300 spa, and dru data. This information and year of isolation
and other non–ST239 infections are shown in the Table. are shown in Figure 2. The genotype cluster sizes ranged
Most ST239 isolates were health care–associated MRSA from 2 to 18 isolates; 23 of the isolates were unique. In
and had characteristics and concurrent conditions similar contrast, SNP typing of 22/78 isolates with a panel of
to those associated with USA100. MRSA ST239-III did 43 SNPs showed them to be indistinguishable from each
not have virulent determinants often associated with health other. All isolates tested belonged to haplotype 9 (H9)
care–associated or community-associated MRSA strains, within MRSA ST239-III clade II (Figure 3). This clade
such as PVL, TSST, ACME, or mupA. was composed of isolates from many continents, including
many from sources in Asia (9).
Characteristics of MRSA ST239-III Isolates
Resistance was observed to clindamycin (76/76, Discussion
100%), moxifl oxacin (47/47, 100%), gentamicin (74/77, MRSA ST239-III has demonstrated epidemic potential
96%), tetracycline (70/74, 95%), and trimethoprim– worldwide, and identifi cation of this strain in the United
sulfamethoxazole (62/77, 81%). All MRSA ST239-III States might represent a major public health concern.
isolates were susceptible to vancomycin. For daptomycin, Although the precise time frame of emergence of this
64 (98%) of 65 isolates were susceptible, and 1 blood isolate strain in Ohio is unknown, it appears to have been present
with an MIC of 2 mg/L was classifi ed as uninterpretable. before the study because it was identifi ed in archived
1560 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 10, October 2012