dgkh000176
10.3205/dgkh000176
urn:nbn:de:0183-dgkh0001763
Research Article
MRSA distribution and epidemiological procedures evaluation at two hospitals in Northern Poland
MRSA-Verteilung und epidemiologische Evaluation in zwei Hospitälern in Nordpolen
Paszko
Paszko
Krystyna
K
Department of Clinical Bacteriology, Specialist Hospital, Gdansk, Poland
author
Michnowska
Michnowska
Ewa
E
Department of Clinical Bacteriology, Specialist Hospital, Gdansk, Poland
author
Kurlenda
Kurlenda
Julianna
J
Department of Clinical Bacteriology, Regional Hospital, Koszalin, Poland
author
Grinholc
Grinholc
Mariusz
M
Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, Department of Biotechnology, Laboratory of Molecular Diagnostics, Gdansk, Poland
author
Nakonieczna
Nakonieczna
Joanna
J
Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, Department of Biotechnology, Laboratory of Molecular Diagnostics, Gdansk, Poland
author
Bielawski
Bielawski
Krzysztof Piotr
KP
Prof. Dr.
Intercollegiate Faculty of Biotechnology University of Gdansk and Medical University of Gdansk, Department of Biotechnology, Laboratory of Molecular Diagnostics, Kladki 24, 80-822 Gdansk, Poland, Phone: +48 58 523 63 14, Fax: +48 58 523 64 26Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, Department of Biotechnology, Laboratory of Molecular Diagnostics, Gdansk, Poland
bielawski@biotech.ug.edu.pl
author
German Medical Science GMS Publishing House
Düsseldorf
610
MRSA
screening
incidence
regional comparison
MRSA
Screening
Inzidenz
regionaler Vergleich
20111215
engl
1863-5245
6
1
GMS Krankenhaushygiene Interdisziplinär
GMS Krankenhaushyg Interdiszip
Prevention and therapy of nosocomial infections
19
In der Studie wurde der Einfluss eines modifizierten MRSA-Screenings bei Trägern und Patienten auf die epidemiologische Situation von MRSA in zwei ähnlichen regionalen Krankenhäusern in Nordpolen im Zeitraum 2008–2010 analysiert. Unabhängig von der unterschiedlichen Strategie der Prävention und Intervention in beiden Krankenhäusern dürfte die unterschiedliche MRSA-Inzidenz regional begründet sein.
In the present study we have analyzed the impact of modified MRSA screening of carriers and patients on epidemiological situation of MRSA during 2008–2010, comparing two regional hospitals with similar bed numbers and similar ward profiles in Northern Poland. In 2008 the proportion of MRSA to all S. aureus isolates was 14.4% resp. 6.0%, in 2009 8.3% resp. 4.7% and in 2010 6.5% in both hospitals. Independent of the different prevention and intervention strategy in both hospitals the different MRSA incidence seems to be due to regional epidemic settings
IntroductionMethicillin resistant Staphylococcus aureus (MRSA) is one of the most common pathogens responsible for hospital infections and, as recently discovered, also for community acquired infections. It can cause a broad spectrum of infections through local invasion, toxin mediated diseases to generalized infections. S. aureus is a bacterium commonly present in the human population and constant or part time carrier frequency in the nasal vestibule is estimated at 30–60% , , , . Therapeutic problems are mainly caused by infections with strains, which are resistant not only to methicillin (methicillin-resistant S. aureus, MRSA) and in consequence to all β-lactam antibiotics but also to many other group of antimicrobial therapeutics. The presence of this pathogen enables its local distribution e.g. within a hospital ward and/or between hospital wards (hospital or healthcare acquired) HA-MRSA , , , , . When such a strain carries genes responsible for the resistance to many antibiotics, as in the in case of HA-MRSA strains , , , , , ; then it becomes a great problem both, therapeutically – due to the limited number of antibiotics available, as well as economically – due to the necessity of expensive drugs and the prolonged time spent in the hospital , , , , , , . The increase of costs is also a result of special procedure initiations needed for controlling the wide-spread of the pathogen, such as hygienic and isola<![CDATA[tion</PlainText></TextGroup> procedures, identifying the carrier and, next, its eradication <TextLink reference="1"></TextLink>, <TextLink reference="13"></TextLink>, <TextLink reference="17"></TextLink>. In some countries MRSA can constitute up to 80% of all <Mark2>S. aureus</Mark2> isolates in hospitals <TextLink reference="14"></TextLink>. In some Polish hospitals the percentage of MRSA strains reached up to ~60% <TextLink reference="20"></TextLink>. The frequency of bacteremia of this etiology, according to research carried out in the years 1999–2000 in Europe, depending on the country ranged from 44.4% (Greece) to 0.6% (Denmark and the Netherlands) <TextLink reference="24"></TextLink>. According to the research of SENTRY carried out in the years 1997–1999 in USA, Canada, Latin America, and Western Pacific, the percentage of infection in these areas was 25.3; 19.2; 20.6 and 21.6, respectively <TextLink reference="3"></TextLink>. In our study we have analyzed the impact of modified procedures on epidemiological situation of MRSA during the last three years comparing two similar hospitals in Northern Poland.</Pgraph></TextBlock>
<TextBlock linked="yes" name="Material and methods">
<MainHeadline>Material and methods</MainHeadline><Pgraph>A three-year-lasting period (2008–2010) was analyzed. Only the first isolate from one patient and no duplicate were taken into account.</Pgraph><SubHeadline>Hospital no. 1 </SubHeadline><Pgraph>Gdansk is the city that lies on the southern edge of Gdansk Bay (of the Baltic Sea), in a conurbation with the city of Gdynia, spa town of Sopot, and suburban communities, which together form a metropolitan area called the Tricity (<Mark2>Trójmiasto</Mark2>), with a population of over 800,000. Gdansk itself has a population of 455,830 (June 2010), making it the largest city in the Pomerania region of Northern Poland.</Pgraph><Pgraph>The 608-bed regional hospital contains three internal departments, cardiology, neurology, pediatric ward, surgery, orthopedic, ICU (adult), ICU neonatal, obstetrics and gynecology, neonatology, laryngology, ophthalmic ward and dialysis unit. The yearly admittance rate and average hospitalization time are presented in Table 1 <ImgLink imgNo="1" imgType="table"/> and <TextGroup><PlainText>Table 2 </PlainText></TextGroup><ImgLink imgNo="2" imgType="table"/>. Population of the citizens with access to this hospital is estimated on the level of 205,000.</Pgraph><Pgraph>Bacteriology lab has an access to the analytical software WHONET (WHO) and VITEK (BioMerieux, France).</Pgraph><Pgraph>The modified epidemiological procedure concerning MRSA carriers and patients (Procedure 1) has been implemented within the hospital.</Pgraph><Pgraph>Procedure 1 is characterized by the following criteria:</Pgraph><Pgraph><UnorderedList><ListItem level="1">Epidemiological procedure concerning initial MRSA, VISA or VRSA isolation.</ListItem><ListItem level="1">Patient suspected of being infected (colonized) with MRSA, should be placed in a separate room, may be provided with other patients who have had the presence of a strain.</ListItem><ListItem level="1">The patients prescribed to eradication treatment should not be cohorted. </ListItem><ListItem level="1">The epidemiological investigation is being performed to determine the origin of the strain.</ListItem><ListItem level="1">In the case of hospital-acquired infections, the high-risk patients are being screened with microbiological tests (nasal-throat, respiratory tract and rectal isola<TextGroup><PlainText>tions</PlainText></TextGroup>).</ListItem><ListItem level="1">The employed medical staff is trained over the prophylaxis of MRSA, VISA and VRSA infections.</ListItem><ListItem level="1">The verification of the established epidemiological procedures is performed. </ListItem></UnorderedList></Pgraph><SubHeadline>Hospital no. 2 </SubHeadline><Pgraph>Koszalin is the largest city of Middle Pomerania in north-western Poland, possess a county-status city and is a capital of Koszalin County of West Pomeranian Voivodeship since 1999. Previously, it was a capital of Koszalin Voivodeship (1950–1998). Population of the citizens with access to this hospital is estim<TextGroup><PlainText>ated</PlainText></TextGroup> on the level of 650,000 and Koszalin itself has a population of 107,217 (2009).</Pgraph><Pgraph>The 609-bed regional hospital contains two internal wards, cardiology, neurology, oncology, infectious diseases ward, pediatric, children surgery, general surgery, orthopedic, ICU (adult), ICU neonatal, obstetrics and gynecology, neonatology, laryngology, ophthalmic ward, dermatology and dialysis unit. The hospital characteristics have been presented in Table 3 <ImgLink imgNo="3" imgType="table"/> and Table 4 <ImgLink imgNo="4" imgType="table"/>.</Pgraph><Pgraph>Bacteriology lab has an access to the analytical software Marcel.</Pgraph><Pgraph>The modified epidemiological procedure concerning MRSA carriers and patients (Procedure 2) has been employed implemented in the hospital.</Pgraph><Pgraph>Procedure 2 is characterized by the following criteria:</Pgraph><Pgraph><UnorderedList><ListItem level="1">Procedure of treatment of patients suspected of MRSA infection, infected (colonized) with MRSA (Methicillin Resistant <Mark2>Staphylococcus aureus</Mark2>), VRSA (Vancomycin Resistant <Mark2>Staphylococcus aureus</Mark2>), VRE (Vancomycin Resistant Enterococci) refers to medical staff, supporting staff, staff of hospital hygiene</ListItem><ListItem level="1">Patient suspected of being infected (colonized) with MRSA should be placed in a separate room, may be provided with other patients who have had the presence of a strain</ListItem><ListItem level="1">Room equipped with items and equipment as the standard isolation of infections spreading through direct contact</ListItem><UnorderedList><ListItem level="2">indicated the use of single sheets</ListItem></UnorderedList><UnorderedList><ListItem level="2">in the case of reusable application, one should proceed as in terms of dirty sheets</ListItem></UnorderedList><ListItem level="1">Room doors must be closed</ListItem><ListItem level="1">Medical and hospital hygiene staff are informed on the reason of isolation</ListItem><ListItem level="1">One entering the room should put on</ListItem><UnorderedList><ListItem level="2">disposable protective – apron, shoe pads, cap on head</ListItem></UnorderedList><UnorderedList><ListItem level="2">disposable non-sterile gloves for nursing activities, sterile for aseptic operations</ListItem></UnorderedList><UnorderedList><ListItem level="2">surgical mask in case of carrying of MRSA/VRSA/VRE in patient's airway</ListItem></UnorderedList><UnorderedList><ListItem level="2">before leaving the room take off personal protective equipment and place in red bag</ListItem></UnorderedList><UnorderedList><ListItem level="2">before performing the steps, in the course if necessary, and upon completion, the procedure for hygienic hand-washing applies</ListItem></UnorderedList><ListItem level="1">Mandatory reporting by consultants (visiting family) to a designated nurse to obtain information about safety precautions</ListItem><UnorderedList><ListItem level="2">avoidance of unnecessary traffic in the hall of the isolation ward</ListItem></UnorderedList><UnorderedList><ListItem level="2">restriction of movements of the patient in the ward and outside – full information about the precautionary measures</ListItem></UnorderedList><ListItem level="1">Wasted disposable equipment, dressings, etc. are subject to proceedings according to the instruction of medical waste</ListItem><ListItem level="1">Reusable equipment is subject to disinfection processes, cleaning and sterilization</ListItem><ListItem level="1">Dealing with surfaces contaminated with biological material in accordance with the procedure for the safety and handling of infectious material</ListItem><ListItem level="1">Hygienic treatment of patient:</ListItem><UnorderedList><ListItem level="2">the entire body must be washed daily with an antiseptic for this purpose, hair shampoo 2x a week</ListItem></UnorderedList><UnorderedList><ListItem level="2">the patient's bedding and linen change every day, following the steps “on-bed” bedside management of patient</ListItem></UnorderedList><ListItem level="1">Cleaning the room twice a day and depending on the needs</ListItem><ListItem level="1">In order to identify carriers and patients infected with MRSA/VRSA material for microbiological examination should be collected from the nasal vestibule or perineum, or groin, or areas of the affected skin; material for a directed search towards VRE identification should be sampled from the anal area (or a stool sample) or the perineum, lesions of the damaged skin or the cathetered patient's urine sample</ListItem><ListItem level="1">Patients, who have had contact with microbiologically diagnosed MRSA/VRSA/VRE infected patient or MRSA/VRSA/VRE carrier, should be cohorted</ListItem><ListItem level="1">If a patient is diagnosed as MRSA/VRSA/VRE carrier and if allowed by the clinical condition, the patient should be discharged with recommendations for further treatment aimed at eliminating the carrier state-control swabs should be taken for at least 5 days after the procedure eliminating carrier state; it is advisable to obtain a 3-time negative results</ListItem><ListItem level="1">The re-taking of the patient to the hospital or taking a patient previously hospitalized in other wards/hosp<TextGroup><PlainText>itals</PlainText></TextGroup>, where endemic or epidemic presence of MRSA/VRSA/VRE was recorded, it is advisable to carry out directed microbial diagnostics; until the results are obtained, strict adherence to the principles of insulation of directly transmitted infections must be applied</ListItem><ListItem level="1">Staff colonized with MRSA/VRSA/VRE should be removed from contact with patients, until elimination of the carrier state; before taking the job a microbiological control of the MRSA/VRSA/VRE carrier state should be performed, especially in the personnel previously employed in hospitals where the MRSA/VRSA/VRE were registered.</ListItem></UnorderedList></Pgraph></TextBlock>
<TextBlock linked="yes" name="Results">
<MainHeadline>Results</MainHeadline><Pgraph>According to comparative analysis performed for two regional hospitals of Northern Poland with similar bed numbers (608 vs. 609) and similar ward profiles, the percentage of MRSA distribution was different. In 2008 at hospital no. 1 the rate of MRSA to all <Mark2>S. aureus</Mark2> isolates was 14.4% and at hospital no. 2 the same rate was 6.0%. In 2009 these rates were 8.3% and 4.7%, respectively. However, in 2010, the rate was similar for the two described hospitals (Table 2 <ImgLink imgNo="2" imgType="table"/> and Table 4 <ImgLink imgNo="4" imgType="table"/>). The differences concern also the number of hospitalized patients, hospitalization time and number of microbiological tests performed (Table 1 <ImgLink imgNo="1" imgType="table"/> and Table 3 <ImgLink imgNo="3" imgType="table"/>). At hospital no. 1 the number of hospitalized patients was approx. 25,000, the hospitalization time was 6.6–6.7 days with percentage of patients’ beds occupation of approx. 75%. At hospital no. 2 the number of hospitalized patients was higher – ca. 31,000, nevertheless the average hospitalization time was shorter and was calculated as 4.6–4.9 days with lower percentage of patients’ beds occupation (62.3–68.2%). The high difference concerns also the number of microbiological specimens. At hospital no. 1, the number of specimens/100 patients was as follows: in 2008 – 101.9, in 2009 – 110.7 and in 2010 – 122.7. At hospital no. 2 much smaller number of specimens/100 patients was performed in each year: 29.51, 32.1 and 45.6, respectively.</Pgraph></TextBlock>
<TextBlock linked="yes" name="Discussion">
<MainHeadline>Discussion</MainHeadline><Pgraph>In the last decade in Poland, the monitoring of MRSA infections and carriers has been improved <TextLink reference="11"></TextLink>, <TextLink reference="16"></TextLink>. Previously some health-associated centers introduced the survey, and epidemiological procedures concerning MRSA carriers and patients <TextLink reference="11"></TextLink>, <TextLink reference="13"></TextLink>, <TextLink reference="18"></TextLink>. Currently, many hospitals in Poland are involved within the European project EARS-Net (<Hyperlink href="http://ecdc.europa.eu/en/activities/surveillance/EARS-Net/">http://ecdc.europa.eu/en/activities/surveillance/EARS-Net/</Hyperlink>), what enables in future the unification of procedures and surveillance methods. Nowadays, each medical center forms its own procedures on the basis of obtained results from epidemiological investigations. Both of described hospitals have already been involved within the above-mentioned project. It is clearly visible that the comparison of even very similar hospitals is quite difficult. Twice more isolations of MRSA in 2008 at hospital no. 1 could result from regional epidemic settings. In that time one outbreak in internal was noticed (4 infected patients, 1 carrier). Relatively, in hospital no. 2 in the same year in spite of a lower number of specimens send for bacteriological analysis, there were more isolations of <Mark2>S. aureus</Mark2> (533 vs. 478) and smaller number of isolation of MRSA with one outbreak in neurology ward (4 infected patients and 9 carriers). Though the percentage of MRSA in 2010 year was slightly higher (6.5%), we have observed the decrease of MRSA hospital-acquired infections from 3 and 4 in 2008–2009 to 0 in 2010. It is interesting that in both hospitals the number of specimens send to bacteriology lab consequently increased whereas the frequency of MRSA isolations decreased. In our opinion, it results from effective and properly used procedures of MRSA surveillance. This opinion could be supported by results from EARS-Net report where overall in Poland MRSA isolation frequency in 2009 is 20% (<Hyperlink href="http://ecdc.europa.eu/en/activities/surveillance/EARS-Net/">http://ecdc.europa.eu/en/activities/surveillance/EARS-Net/</Hyperlink>).</Pgraph></TextBlock>
<TextBlock linked="yes" name="Notes">
<MainHeadline>Notes</MainHeadline><SubHeadline>Conflicts of interest</SubHeadline><Pgraph>The authors declare that they have no competing interests.</Pgraph></TextBlock>
<References linked="yes">
<Reference refNo="1">
<RefAuthor>Coia JE</RefAuthor>
<RefAuthor>Duckworth GJ</RefAuthor>
<RefAuthor>Edwards DI</RefAuthor>
<RefAuthor>Farrington M</RefAuthor>
<RefAuthor>Fry C</RefAuthor>
<RefAuthor>Humphreys H</RefAuthor>
<RefAuthor>Mallaghan C</RefAuthor>
<RefAuthor>Tucker DR</RefAuthor>
<RefAuthor> Joint Working Party of the British Society of Antimicrobial Chemotherapy</RefAuthor>
<RefAuthor> Hospital Infection Society</RefAuthor>
<RefAuthor> Infection Control Nurses Association</RefAuthor>
<RefTitle>Guidelines for the control and prevention of meticillin-resistant Staphylococcus aureus (MRSA) in healthcare facilities</RefTitle>
<RefYear>2006</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>S1-44</RefPage>
<RefTotal>Coia JE, Duckworth GJ, Edwards DI, Farrington M, Fry C, Humphreys H, Mallaghan C, Tucker DR; Joint Working Party of the British Society of Antimicrobial Chemotherapy; Hospital Infection Society; Infection Control Nurses Association. Guidelines for the control and prevention of meticillin-resistant Staphylococcus aureus (MRSA) in healthcare facilities. J Hosp Infect. 2006;63 (Suppl 1):S1-44</RefTotal>
</Reference>
<Reference refNo="2">
<RefAuthor>Conceição T</RefAuthor>
<RefAuthor>Aires-de-Sousa M</RefAuthor>
<RefAuthor>Füzi M</RefAuthor>
<RefAuthor>Tóth A</RefAuthor>
<RefAuthor>Pászti J</RefAuthor>
<RefAuthor>Ungvári E</RefAuthor>
<RefAuthor>van Leeuwen WB</RefAuthor>
<RefAuthor>van Belkum A</RefAuthor>
<RefAuthor>Grundmann H</RefAuthor>
<RefAuthor>de Lencastre H</RefAuthor>
<RefTitle>Replacement of methicillin-resistant Staphylococcus aureus clones in Hungary over time: a 10-year surveillance study</RefTitle>
<RefYear>2007</RefYear>
<RefJournal>Clin Microbiol Infect</RefJournal>
<RefPage>971-9</RefPage>
<RefTotal>Conceição T, Aires-de-Sousa M, Füzi M, Tóth A, Pászti J, Ungvári E, van Leeuwen WB, van Belkum A, Grundmann H, de Lencastre H. Replacement of methicillin-resistant Staphylococcus aureus clones in Hungary over time: a 10-year surveillance study. Clin Microbiol Infect. 2007;13(10):971-9. DOI: 10.1111/j.1469-0691.2007.01794.x</RefTotal>
<RefLink>http://dx.doi.org/10.1111/j.1469-0691.2007.01794.x</RefLink>
</Reference>
<Reference refNo="3">
<RefAuthor>Diekema DJ</RefAuthor>
<RefAuthor>Pfaller MA</RefAuthor>
<RefAuthor>Schmitz FJ</RefAuthor>
<RefAuthor>Smayevsky J</RefAuthor>
<RefAuthor>Bell J</RefAuthor>
<RefAuthor>Jones RN</RefAuthor>
<RefAuthor>Beach M</RefAuthor>
<RefAuthor> SENTRY Partcipants Group</RefAuthor>
<RefTitle>Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997–1999</RefTitle>
<RefYear>2001</RefYear>
<RefJournal>Clin Infect Dis</RefJournal>
<RefPage>S114-32</RefPage>
<RefTotal>Diekema DJ, Pfaller MA, Schmitz FJ, Smayevsky J, Bell J, Jones RN, Beach M; SENTRY Partcipants Group. Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997–1999. Clin Infect Dis. 2001;32 (Suppl 2):S114-32. DOI: 10.1086/320184</RefTotal>
<RefLink>http://dx.doi.org/10.1086/320184</RefLink>
</Reference>
<Reference refNo="4">
<RefAuthor>Dzwonkowska J</RefAuthor>
<RefAuthor>Kurlenda J</RefAuthor>
<RefAuthor>Baczkowski B</RefAuthor>
<RefAuthor>Mazurkiewicz S</RefAuthor>
<RefAuthor>Uzunov I</RefAuthor>
<RefAuthor>Ziólkowski W</RefAuthor>
<RefAuthor>Markowicz A</RefAuthor>
<RefTitle>The effect of antibiotic therapy on the incidence of Staphylococcus aureus infections in orthopaedic patients</RefTitle>
<RefYear>2007</RefYear>
<RefJournal>Ortop Traumatol Rehabil</RefJournal>
<RefPage>532-47</RefPage>
<RefTotal>Dzwonkowska J, Kurlenda J, Baczkowski B, Mazurkiewicz S, Uzunov I, Ziólkowski W, Markowicz A. The effect of antibiotic therapy on the incidence of Staphylococcus aureus infections in orthopaedic patients. Ortop Traumatol Rehabil. 2007;9(5):532-47.</RefTotal>
</Reference>
<Reference refNo="5">
<RefAuthor>Finch R</RefAuthor>
<RefTitle>Gram-positive infections: lessons learnt and novel solutions</RefTitle>
<RefYear>2006</RefYear>
<RefJournal>Clin Microbiol Infect</RefJournal>
<RefPage>3-8</RefPage>
<RefTotal>Finch R. Gram-positive infections: lessons learnt and novel solutions. Clin Microbiol Infect. 2006;12:3-8. DOI: 10.1111/j.1469-0691.2006.01624.x</RefTotal>
<RefLink>http://dx.doi.org/10.1111/j.1469-0691.2006.01624.x</RefLink>
</Reference>
<Reference refNo="6">
<RefAuthor>Graham PL 3rd</RefAuthor>
<RefAuthor>Lin SX</RefAuthor>
<RefAuthor>Larson EL</RefAuthor>
<RefTitle>A U.S. population-based survey of Staphylococcus aureus colonization</RefTitle>
<RefYear>2006</RefYear>
<RefJournal>Ann Intern Med</RefJournal>
<RefPage>318-25</RefPage>
<RefTotal>Graham PL 3rd, Lin SX, Larson EL. A U.S. population-based survey of Staphylococcus aureus colonization. Ann Intern Med. 2006;144(5):318-25.</RefTotal>
</Reference>
<Reference refNo="7">
<RefAuthor>Huang YH</RefAuthor>
<RefAuthor>Tseng SP</RefAuthor>
<RefAuthor>Hu JM</RefAuthor>
<RefAuthor>Tsai JC</RefAuthor>
<RefAuthor>Hsueh PR</RefAuthor>
<RefAuthor>Teng LJ</RefAuthor>
<RefTitle>Clonal spread of SCCmec type IV methicillin-resistant Staphylococcus aureus between community and hospital</RefTitle>
<RefYear>2007</RefYear>
<RefJournal>Clin Microbiol Infect</RefJournal>
<RefPage>717-24</RefPage>
<RefTotal>Huang YH, Tseng SP, Hu JM, Tsai JC, Hsueh PR, Teng LJ. Clonal spread of SCCmec type IV methicillin-resistant Staphylococcus aureus between community and hospital. Clin Microbiol Infect. 2007;13(7):717-24. DOI: 10.1111/j.1469-0691.2007.01718.x</RefTotal>
<RefLink>http://dx.doi.org/10.1111/j.1469-0691.2007.01718.x</RefLink>
</Reference>
<Reference refNo="8">
<RefAuthor>Kalmeijer MD</RefAuthor>
<RefAuthor>van Nieuwland-Bollen E</RefAuthor>
<RefAuthor>Bogaers-Hofman D</RefAuthor>
<RefAuthor>de Baere GA</RefAuthor>
<RefTitle>Nasal carriage of Staphylococcus aureus is a major risk factor for surgical-site infections in orthopedic surgery</RefTitle>
<RefYear>2000</RefYear>
<RefJournal>Infect Control Hosp Epidemiol</RefJournal>
<RefPage>319-23</RefPage>
<RefTotal>Kalmeijer MD, van Nieuwland-Bollen E, Bogaers-Hofman D, de Baere GA. Nasal carriage of Staphylococcus aureus is a major risk factor for surgical-site infections in orthopedic surgery. Infect Control Hosp Epidemiol. 2000;21(5):319-23. DOI: 10.1086/501763</RefTotal>
<RefLink>http://dx.doi.org/10.1086/501763</RefLink>
</Reference>
<Reference refNo="9">
<RefAuthor>Karchmer AW</RefAuthor>
<RefTitle>From theory to practice: resistance in Staphylococcus aureus and new treatments</RefTitle>
<RefYear>2006</RefYear>
<RefJournal>Clin Microbiol Infect</RefJournal>
<RefPage>15-21</RefPage>
<RefTotal>Karchmer AW. From theory to practice: resistance in Staphylococcus aureus and new treatments. Clin Microbiol Infect. 2006;12:15-21. DOI: 10.1111/j.1469-0691.2006.01626.x</RefTotal>
<RefLink>http://dx.doi.org/10.1111/j.1469-0691.2006.01626.x</RefLink>
</Reference>
<Reference refNo="10">
<RefAuthor>Karchmer TB</RefAuthor>
<RefAuthor>Durbin LJ</RefAuthor>
<RefAuthor>Simonton BM</RefAuthor>
<RefAuthor>Farr BM</RefAuthor>
<RefTitle>Cost-effectiveness of active surveillance cultures and contact/droplet precautions for control of methicillin-resistant Staphylococcus aureus</RefTitle>
<RefYear>2002</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>126-32</RefPage>
<RefTotal>Karchmer TB, Durbin LJ, Simonton BM, Farr BM. Cost-effectiveness of active surveillance cultures and contact/droplet precautions for control of methicillin-resistant Staphylococcus aureus. J Hosp Infect. 2002;51(2):126-32. DOI: 10.1053/jhin.2002.1200</RefTotal>
<RefLink>http://dx.doi.org/10.1053/jhin.2002.1200</RefLink>
</Reference>
<Reference refNo="11">
<RefAuthor>Karynski M</RefAuthor>
<RefAuthor>Sabat AJ</RefAuthor>
<RefAuthor>Empel J</RefAuthor>
<RefAuthor>Hryniewicz W</RefAuthor>
<RefTitle>Molecular surveillance of methicillin-resistant Staphylococcus aureus by multiple-locus variable number tandem repeat fingerprinting (formerly multiple-locus variable number tandem repeat analysis) and spa typing in a hierarchic approach</RefTitle>
<RefYear>2008</RefYear>
<RefJournal>Diagn Microbiol Infect Dis</RefJournal>
<RefPage>255-62</RefPage>
<RefTotal>Karynski M, Sabat AJ, Empel J, Hryniewicz W. Molecular surveillance of methicillin-resistant Staphylococcus aureus by multiple-locus variable number tandem repeat fingerprinting (formerly multiple-locus variable number tandem repeat analysis) and spa typing in a hierarchic approach. Diagn Microbiol Infect Dis. 2008;62(3):255-62. DOI: 10.1016/j.diagmicrobio.2008.06.019</RefTotal>
<RefLink>http://dx.doi.org/10.1016/j.diagmicrobio.2008.06.019</RefLink>
</Reference>
<Reference refNo="12">
<RefAuthor>Kuint J</RefAuthor>
<RefAuthor>Barzilai A</RefAuthor>
<RefAuthor>Regev-Yochay G</RefAuthor>
<RefAuthor>Rubinstein E</RefAuthor>
<RefAuthor>Keller N</RefAuthor>
<RefAuthor>Maayan-Metzger A</RefAuthor>
<RefTitle>Comparison of community-acquired methicillin-resistant Staphylococcus aureus bacteremia to other staphylococcal species in a neonatal intensive care unit</RefTitle>
<RefYear>2007</RefYear>
<RefJournal>Eur J Pediatr</RefJournal>
<RefPage>319-25</RefPage>
<RefTotal>Kuint J, Barzilai A, Regev-Yochay G, Rubinstein E, Keller N, Maayan-Metzger A. Comparison of community-acquired methicillin-resistant Staphylococcus aureus bacteremia to other staphylococcal species in a neonatal intensive care unit. Eur J Pediatr. 2007;166(4):319-25. DOI: 10.1007/s00431-006-0238-5</RefTotal>
<RefLink>http://dx.doi.org/10.1007/s00431-006-0238-5</RefLink>
</Reference>
<Reference refNo="13">
<RefAuthor>Kurlenda J</RefAuthor>
<RefAuthor>Grinholc M</RefAuthor>
<RefAuthor>Jasek K</RefAuthor>
<RefAuthor>Wegrzyn G</RefAuthor>
<RefTitle>RAPD typing of methicillin-resistant Staphylococcus aureus: a 7-year experience in a Polish hospital</RefTitle>
<RefYear>2007</RefYear>
<RefJournal>Med Sci Monit</RefJournal>
<RefPage>MT13-8</RefPage>
<RefTotal>Kurlenda J, Grinholc M, Jasek K, Wegrzyn G. RAPD typing of methicillin-resistant Staphylococcus aureus: a 7-year experience in a Polish hospital. Med Sci Monit. 2007;13(6):MT13-8.</RefTotal>
</Reference>
<Reference refNo="14">
<RefAuthor>Leski T</RefAuthor>
<RefAuthor>Oliveira D</RefAuthor>
<RefAuthor>Trzcinski K</RefAuthor>
<RefAuthor>Sanches IS</RefAuthor>
<RefAuthor>Aires de Sousa M</RefAuthor>
<RefAuthor>Hryniewicz W</RefAuthor>
<RefAuthor>de Lencastre H</RefAuthor>
<RefTitle>Clonal distribution of methicillin-resistant Staphylococcus aureus in Poland</RefTitle>
<RefYear>1998</RefYear>
<RefJournal>J Clin Microbiol</RefJournal>
<RefPage>3532-9</RefPage>
<RefTotal>Leski T, Oliveira D, Trzcinski K, Sanches IS, Aires de Sousa M, Hryniewicz W, de Lencastre H. Clonal distribution of methicillin-resistant Staphylococcus aureus in Poland. J Clin Microbiol. 1998;36(12):3532-9.</RefTotal>
</Reference>
<Reference refNo="15">
<RefAuthor>Livermore DM</RefAuthor>
<RefTitle>Can beta-lactams be re-engineered to beat MRSA?</RefTitle>
<RefYear>2006</RefYear>
<RefJournal>Clin Microbiol Infect</RefJournal>
<RefPage>11-6</RefPage>
<RefTotal>Livermore DM. Can beta-lactams be re-engineered to beat MRSA? Clin Microbiol Infect. 2006;12 Suppl 2:11-6. DOI: 10.1111/j.1469-0691.2006.01403.x</RefTotal>
<RefLink>http://dx.doi.org/10.1111/j.1469-0691.2006.01403.x</RefLink>
</Reference>
<Reference refNo="16">
<RefAuthor>Luczak-Kadlubowska A</RefAuthor>
<RefAuthor>Sulikowska A</RefAuthor>
<RefAuthor>Empel J</RefAuthor>
<RefAuthor>Piasecka A</RefAuthor>
<RefAuthor>Orczykowska M</RefAuthor>
<RefAuthor>Kozinska A</RefAuthor>
<RefAuthor>Hryniewicz W</RefAuthor>
<RefTitle>Countrywide molecular survey of methicillin resistant Staphylococcus aureus strains in Poland</RefTitle>
<RefYear>2008</RefYear>
<RefJournal>J Clin Microbiol</RefJournal>
<RefPage>2930-7</RefPage>
<RefTotal>Luczak-Kadlubowska A, Sulikowska A, Empel J, Piasecka A, Orczykowska M, Kozinska A, Hryniewicz W. Countrywide molecular survey of methicillin resistant Staphylococcus aureus strains in Poland. J Clin Microbiol. 2008;46(9):2930-7. DOI: 10.1128/JCM.00869-08</RefTotal>
<RefLink>http://dx.doi.org/10.1128/JCM.00869-08</RefLink>
</Reference>
<Reference refNo="17">
<RefAuthor>Marshall C</RefAuthor>
<RefAuthor>Wolfe R</RefAuthor>
<RefAuthor>Kossmann T</RefAuthor>
<RefAuthor>Wesselingh S</RefAuthor>
<RefAuthor>Harrington G</RefAuthor>
<RefAuthor>Spelman D</RefAuthor>
<RefTitle>Risk factors for acquisition of methicillin-resistant Staphylococcus aureus (MRSA) by trauma patients in the intensive care unit</RefTitle>
<RefYear>2004</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>245-52</RefPage>
<RefTotal>Marshall C, Wolfe R, Kossmann T, Wesselingh S, Harrington G, Spelman D. Risk factors for acquisition of methicillin-resistant Staphylococcus aureus (MRSA) by trauma patients in the intensive care unit. J Hosp Infect. 2004;57(3):245-52. DOI: 10.1016/j.jhin.2004.03.024</RefTotal>
<RefLink>http://dx.doi.org/10.1016/j.jhin.2004.03.024</RefLink>
</Reference>
<Reference refNo="18">
<RefAuthor>Matynia B</RefAuthor>
<RefAuthor>Mlodzinska E</RefAuthor>
<RefAuthor>Hryniewicz W</RefAuthor>
<RefTitle>Antimicrobial susceptibility patterns of Staphylococcus aureus in Poland obtained by the National Quality Assurance Programme</RefTitle>
<RefYear>2005</RefYear>
<RefJournal>Clin Microbiol Infect</RefJournal>
<RefPage>379-85</RefPage>
<RefTotal>Matynia B, Mlodzinska E, Hryniewicz W. Antimicrobial susceptibility patterns of Staphylococcus aureus in Poland obtained by the National Quality Assurance Programme. Clin Microbiol Infect. 2005;11(5):379-85. DOI: 10.1111/j.1469-0691.2005.01105.x</RefTotal>
<RefLink>http://dx.doi.org/10.1111/j.1469-0691.2005.01105.x</RefLink>
</Reference>
<Reference refNo="19">
<RefAuthor>Pan ES</RefAuthor>
<RefAuthor>Diep BA</RefAuthor>
<RefAuthor>Charlebois ED</RefAuthor>
<RefAuthor>Auerswald C</RefAuthor>
<RefAuthor>Carleton HA</RefAuthor>
<RefAuthor>Sensabaugh GF</RefAuthor>
<RefAuthor>Perdreau-Remington F</RefAuthor>
<RefTitle>Population dynamics of nasal strains of methicillin-resistant Staphylococcus aureus – and their relation to community-associated disease activity</RefTitle>
<RefYear>2005</RefYear>
<RefJournal>J Infect Dis</RefJournal>
<RefPage>811-8</RefPage>
<RefTotal>Pan ES, Diep BA, Charlebois ED, Auerswald C, Carleton HA, Sensabaugh GF, Perdreau-Remington F. Population dynamics of nasal strains of methicillin-resistant Staphylococcus aureus – and their relation to community-associated disease activity. J Infect Dis. 2005;192(5):811-8. DOI: 10.1086/432072</RefTotal>
<RefLink>http://dx.doi.org/10.1086/432072</RefLink>
</Reference>
<Reference refNo="20">
<RefAuthor>Piechowicz L</RefAuthor>
<RefAuthor>Namysl E</RefAuthor>
<RefAuthor>Galinski J</RefAuthor>
<RefTitle>Wystepowanie metycylinoopornych gronkowcow w Polsce i ich charakterystyka</RefTitle>
<RefYear>1993</RefYear>
<RefJournal>Med Dosw Mikrobiol</RefJournal>
<RefPage>273-6</RefPage>
<RefTotal>Piechowicz L, Namysl E, Galinski J. Wystepowanie metycylinoopornych gronkowcow w Polsce i ich charakterystyka [Occurrence of methicillin-resistant strains in Poland and their characteristics]. Med Dosw Mikrobiol. 1993;45(3):273-6.</RefTotal>
</Reference>
<Reference refNo="21">
<RefAuthor>Rayner C</RefAuthor>
<RefAuthor>Munckhof WJ</RefAuthor>
<RefTitle>Antibiotics currently used in the treatment of infections caused by Staphylococcus aureus</RefTitle>
<RefYear>2005</RefYear>
<RefJournal>Intern Med J</RefJournal>
<RefPage>S3-16</RefPage>
<RefTotal>Rayner C, Munckhof WJ. Antibiotics currently used in the treatment of infections caused by Staphylococcus aureus. Intern Med J. 2005;35 (Suppl 2):S3-16. DOI: 10.1111/j.1444-0903.2005.00976.x</RefTotal>
<RefLink>http://dx.doi.org/10.1111/j.1444-0903.2005.00976.x</RefLink>
</Reference>
<Reference refNo="22">
<RefAuthor>Savas L</RefAuthor>
<RefAuthor>Duran N</RefAuthor>
<RefAuthor>Onlen Y</RefAuthor>
<RefAuthor>Savas N</RefAuthor>
<RefAuthor>Erayman M</RefAuthor>
<RefTitle>Prospective analysis of antibiotic susceptibility patterns of MRSA in a Turkish University Hospital</RefTitle>
<RefYear>2005</RefYear>
<RefJournal>Turk J Med Sci</RefJournal>
<RefPage>323-7</RefPage>
<RefTotal>Savas L, Duran N, Onlen Y, Savas N, Erayman M. Prospective analysis of antibiotic susceptibility patterns of MRSA in a Turkish University Hospital. Turk J Med Sci. 2005;35:323-7.</RefTotal>
</Reference>
<Reference refNo="23">
<RefAuthor>Sola C</RefAuthor>
<RefAuthor>Gribaudo G</RefAuthor>
<RefAuthor>Vindel A</RefAuthor>
<RefAuthor>Patrito L</RefAuthor>
<RefAuthor>Bocco JL</RefAuthor>
<RefAuthor> Córdoba MRSA Collaborative Study Group</RefAuthor>
<RefTitle>Identification of a novel methicillin-resistant Staphylococcus aureus epidemic clone in Córdoba, Argentina, involved in nosocomial infections</RefTitle>
<RefYear>2002</RefYear>
<RefJournal>J Clin Microbiol</RefJournal>
<RefPage>1427-35</RefPage>
<RefTotal>Sola C, Gribaudo G, Vindel A, Patrito L, Bocco JL; Córdoba MRSA Collaborative Study Group. Identification of a novel methicillin-resistant Staphylococcus aureus epidemic clone in Córdoba, Argentina, involved in nosocomial infections. J Clin Microbiol. 2002;40(4):1427-35. DOI: 10.1128/JCM.40.4.1427-1435.2002</RefTotal>
<RefLink>http://dx.doi.org/10.1128/JCM.40.4.1427-1435.2002</RefLink>
</Reference>
<Reference refNo="24">
<RefAuthor>Tiemersma EW</RefAuthor>
<RefAuthor>Bronzwaer SL</RefAuthor>
<RefAuthor>Lyytikäinen O</RefAuthor>
<RefAuthor>Degener JE</RefAuthor>
<RefAuthor>Schrijnemakers P</RefAuthor>
<RefAuthor>Bruinsma N</RefAuthor>
<RefAuthor>Monen J</RefAuthor>
<RefAuthor>Witte W</RefAuthor>
<RefAuthor>Grundman H</RefAuthor>
<RefAuthor> European Antimicrobial Resistance Surveillance System Participants</RefAuthor>
<RefTitle>Methicillin-resistant Staphylococcus aureus in Europe, 1999-2002</RefTitle>
<RefYear>2004</RefYear>
<RefJournal>Emerg Infect Dis</RefJournal>
<RefPage>1627-34</RefPage>
<RefTotal>Tiemersma EW, Bronzwaer SL, Lyytikäinen O, Degener JE, Schrijnemakers P, Bruinsma N, Monen J, Witte W, Grundman H; European Antimicrobial Resistance Surveillance System Participants. Methicillin-resistant Staphylococcus aureus in Europe, 1999–2002. Emerg Infect Dis. 2004;10(9):1627-34.</RefTotal>
</Reference>
<Reference refNo="25">
<RefAuthor>Trampuz A</RefAuthor>
<RefAuthor>Zimmerli W</RefAuthor>
<RefTitle>Antimicrobial agents in orthopaedic surgery: Prophylaxis and treatment</RefTitle>
<RefYear>2006</RefYear>
<RefJournal>Drugs</RefJournal>
<RefPage>1089-105</RefPage>
<RefTotal>Trampuz A, Zimmerli W. Antimicrobial agents in orthopaedic surgery: Prophylaxis and treatment. Drugs. 2006;66(8):1089-105. DOI: 10.2165/00003495-200666080-00005</RefTotal>
<RefLink>http://dx.doi.org/10.2165/00003495-200666080-00005</RefLink>
</Reference>
<Reference refNo="26">
<RefAuthor>Wertheim HF</RefAuthor>
<RefAuthor>Melles DC</RefAuthor>
<RefAuthor>Vos MC</RefAuthor>
<RefAuthor>van Leeuwen W</RefAuthor>
<RefAuthor>van Belkum A</RefAuthor>
<RefAuthor>Verbrugh HA</RefAuthor>
<RefAuthor>Nouwen JL</RefAuthor>
<RefTitle>The role of nasal carriage in Staphylococcus aureus infections</RefTitle>
<RefYear>2005</RefYear>
<RefJournal>Lancet Infect Dis</RefJournal>
<RefPage>751-62</RefPage>
<RefTotal>Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5(12):751-62. DOI: 10.1016/S1473-3099(05)70295-4</RefTotal>
<RefLink>http://dx.doi.org/10.1016/S1473-3099(05)70295-4</RefLink>
</Reference>
</References>
<Media>
<Tables>
<Table format="png">
<MediaNo>1</MediaNo>
<MediaID>1</MediaID>
<Caption><Pgraph><Mark1>Table 1: The characteristics of the hospital in Gdansk</Mark1></Pgraph></Caption>
</Table>
<Table format="png">
<MediaNo>2</MediaNo>
<MediaID>2</MediaID>
<Caption><Pgraph><Mark1>Table 2: Rate of MRSA isolation (hospital Gdansk)</Mark1></Pgraph></Caption>
</Table>
<Table format="png">
<MediaNo>3</MediaNo>
<MediaID>3</MediaID>
<Caption><Pgraph><Mark1>Table 3: The characteristics of the hospital in Koszalin</Mark1></Pgraph></Caption>
</Table>
<Table format="png">
<MediaNo>4</MediaNo>
<MediaID>4</MediaID>
<Caption><Pgraph><Mark1>Table 4: Rate of MRSA isolation (hospital Koszalin)</Mark1></Pgraph></Caption>
</Table>
<NoOfTables>4</NoOfTables>
</Tables>
<Figures>
<NoOfPictures>0</NoOfPictures>
</Figures>
<InlineFigures>
<NoOfPictures>0</NoOfPictures>
</InlineFigures>
<Attachments>
<NoOfAttachments>0</NoOfAttachments>
</Attachments>
</Media>
</OrigData>
</GmsArticle>]]></plaintext></textgroup></pgraph></textblock></origdata></gmsarticle>