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Original Investigation |

Curbing Methicillin-Resistant Staphylococcus aureus in 38 French Hospitals Through a 15-Year Institutional Control Program FREE

Vincent Jarlier, MD, PhD; David Trystram, MD; Christian Brun-Buisson, MD, PhD; Sandra Fournier, MD; Anne Carbonne, MD; Laurence Marty, MD; Antoine Andremont, MD, PhD; Guillaume Arlet, MD, PhD; Annie Buu-Hoi, MD; Jean Carlet, MD, PhD; Dominique Decré, PharmD, PhD; Serge Gottot, MD, PhD; Laurent Gutmann, MD, PhD; Marie-Laure Joly-Guillou, MD, PhD; Patrick Legrand, MD; Marie-Hélène Nicolas-Chanoine, MD, PhD; Claude-James Soussy, MD, PhD; Michel Wolf, MD, PhD; Jean-Christophe Lucet, MD, PhD; Michelle Aggoune; Gilles Brücker, MD, PhD; Bernard Régnier, MD, PhD; Collégiale de Bactériologie-Virologie-Hygiène des Hôpitaux Universitaires de l’Île de France
[+] Author Affiliations

Author Affiliations: Laboratoire de Bactériologie-Hygiène, Université Pierre et Marie Curie–Paris 6 and Hôpital Pitié–Salpêtrière, Assistance Publique–Hôpitaux de Paris (AP-HP), Paris, France (Drs Jarlier and Trystram); Réanimation Médicale (Dr Brun-Buisson) and Bactériologie-Virologie-Hygiène (Drs Legrand and Soussy), Hôpital Henri Mondor (AP-HP), Créteil, France; Direction de la Politique Médicale (AP-HP), Paris (Drs Jarlier and Fournier); Centre de Coordination de la Lutte Contre les Infections Nosocomiales Paris-Nord (C-CLIN Paris-Nord), Paris (Dr Carbonne and Ms Aggoune); Bactériologie-Virologie-Hygiène, Hôpital de Lagny, Lagny, France (Dr Marty); Bactériologie (Dr Andremont), Santé Publique (Dr Gottot), Unité d’Hygiène (Dr Lucet), and Réanimation Médicale (Drs Wolf and Régnier), Hôpital Bichat–Claude Bernard (AP-HP), Paris; Bactériologie-Virologie-Hygiène, Hôpital Tenon (AP-HP), Paris (Dr Arlet); Bactériologie-Virologie-Hygiène, Hôpital Européen Georges Pompidou (AP-HP), Paris (Dr Buu-Hoi and Gutmann); Direction Médicale, Haute Autorité de Santé, Saint-Denis-La-Plaine, France (Dr Carlet); Bactériologie-Virologie-Hygiène, Hôpital Saint Antoine, Paris (Dr Decré); Bactériologie-Virologie-Hygiène, Centre Hôpitalier Universitaire (CHU) d’Angers, Angers, France (Dr Joly-Guillou); Bactériologie-Virologie-Hygiène, Hôpital Beaujon (AP-HP), Paris (Dr Nicolas-Chanoine); and Direction Médicale, Public Interest Group ESTHER (Ensemble pour une Solidarité Thérapeutique Hospitalière En Réseau), Paris (Dr Brücker).


Arch Intern Med. 2010;170(6):552-559. doi:10.1001/archinternmed.2010.32.
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Background  The Assistance Publique–Hôpitaux de Paris (AP-HP) institution administers 38 teaching hospitals (23 acute care and 15 rehabilitation and long-term care hospitals; total, 23 000 beds) scattered across Paris and surrounding suburbs in France. In the late 1980s, the proportion of methicillin resistance among clinical strains of Staphylococcus aureus (MRSA) reached approximately 40% at AP-HP.

Methods  A program aimed at curbing the MRSA burden was launched in 1993, based on passive and active surveillance, barrier precautions, training, and feedback. This program, supported by the strong commitment of the institution, was reinforced in 2001 by a campaign promoting the use of alcohol-based hand-rub solutions. An observational study on MRSA rate was prospectively carried out from 1993 onwards.

Results  There was a significant progressive decrease in MRSA burden (−35%) from 1993 to 2007, whether recorded as the proportion (expressed as percentage) of MRSA among S aureus strains (41.0% down to 26.6% overall; 45.3% to 24.2% in blood cultures) or incidence of MRSA cases (0.86 down to 0.56 per 1000 hospital days). The MRSA burden decreased more markedly in intensive care units (−59%) than in surgical (−44%) and medical (−32%) wards. The use of ABHR solutions (in liters per 1000 hospital days) increased steadily from 2 L to 21 L (to 26 L in acute care hospitals and to 10 L in rehabilitation and long-term care hospitals) following the campaign.

Conclusion  A sustained reduction of MRSA burden can be obtained at the scale of a large hospital institution with high endemic MRSA rates, providing that an intensive program is maintained for a long period.

Figures in this Article

The rates of methicillin-resistant Staphylococcus aureus (MRSA) have reached high levels during recent decades in many countries all over the world, although some have succeeded in containing the spread of this multidrug-resistant organism.13 Controlling MRSA is a challenge for medical institutions in countries with a high MRSA burden. Because MRSA spread in hospitals is driven by multiple factors such as cross-transmission, invasive procedures, and intensive antibiotic use, all guidelines for MRSA control include bundled measures such as identification and isolation of MRSA carriers, hand hygiene, and antibiotic policy.2,47

In France, the proportion of MRSA in clinical strains of S aureus increased continuously during the 1980s and reached approximately 35% including in blood cultures.814 Such rates became unacceptable after comparative European data were published.15 In response, a long-term program for controlling MRSA was launched in 1993 in the 38 hospitals of the Assistance Publique–Hôpitaux de Paris (AP-HP), the largest public medical institution in France. We present herein the results of an observational incidence study that assessed the positive impact of this large-scale initiative on MRSA rates over a period of 15 years (1993-2007), showing that high endemic rates can be markedly reduced by an intensive long-lasting program.

SETTING

The AP-HP is a public institution that administers 38 teaching hospitals (23 acute care hospitals [ACHs] and 15 rehabilitation and long-term care hospitals [RLTCHs]) scattered across Paris (n = 15) and surrounding suburban counties (n = 23) in France. The AP-HP comprises 23 000 beds (14 300 in ACHs and 8700 in RLTCHs), representing 36% of all the hospital beds in the Paris area (“Île de France”; 11.6 million inhabitants) and 5% of all the beds in France, and admits approximately 1 million patients per year and employs 19 000 physicians, 18 500 nurses, and 29 800 assistant nurses. AP-HP hospitals are managed locally by administrators and medical committees, but decisions on large investments and medical developments are made by the central administration. A local team is in charge of prevention and surveillance of nosocomial infections in each hospital, but actions of foremost importance for the whole institution, such as campaigns for hygiene, are coordinated centrally.

MRSA CONTROL PROGRAM

A program aimed at controlling MRSA was launched in 1993, based on the following objectives:

  • Isolation Interventions: (1) Placement of patients with MRSA infections or colonizations in single-bed rooms whenever possible and (2) barrier precautions for patients with MRSA infections or colonizations such as disposable gloves worn before and discarded after patient contact, disposable aprons worn for extensive contacts (eg, bed making), and small equipment (eg, stethoscope) dedicated to the patient.

  • Promotion of Hand Hygiene: (1) Hand washing with disinfectant soap after contact with patients with MRSA infections or colonizations before leaving the room and (2) an institutional campaign for promoting the use of alcohol-based hand-rub (ABHR) solutions in place of hand washing, launched in 2001 to reinforce the program, which provided pedagogical material to the infection control teams (slide shows, 200 000 brochures, and 14 000 posters) and material on training these teams and sent formal letters by the general director asking all administrators, heads of departments, and chief nurses to support the campaign.

  • Identification of Patients With MRSA Infections or Colonizations: (1) Passive surveillance through routine clinical specimens; (2) active surveillance (screening) by culturing nares swabs when there is a high risk of MRSA colonization, eg, intensive care unit (ICU) patients and contact patients (ie, those hospitalized in the same unit and at the time as patients with MRSA infections); (3) notification of new patients with MRSA infections or colonizations by laboratories to medical teams using quick reporting systems (eg, telephone call) and flags on laboratory reports (“watch MRSA”); (4) identification of patients with MRSA infections using a specific self-sticking label on the door to the patient's room and medical charts; and (5) informing units to which patients with MRSA are transferred.

  • Feedback: Obtaining feedback to the hospital community on the results (MRSA rates and progress in program implementation) at the local level.

STIMULATION OF EFFORTS BY THE INSTITUTION

Since 1998, our institution has further stimulated the efforts by asking each hospital to report annually to the central administration the following selected information on the program, as part of a wider process to promote the quality at AP-HP: (1) size of the infection control team, (2) implementation of the program, (3) organization of audits (eg, on hand hygiene), and (4) feedback. The progress of the initiative has been annually presented during meetings of infection control teams and bacteriologists from all AP-HP hospitals, yielding opportunities to discuss the results, and disseminated within each hospital and central administration.

MRSA SURVEY

To evaluate the impact of the program, a prospective MRSA survey was organized annually from 1993 onwards in AP-HP laboratories, following a standardized protocol. The survey was conducted during the same 6-week period (April to mid-May) from 1993 to 2001, then over 2 full months (April-May) from 2002 to 2004 and over 3 months (April-June) since 2005, to counterbalance the progressive decrease in the number of MRSA cases, given the need to accurately assess the rates of susceptibility to non–β-lactam antibiotics among MRSA strains and the distribution of MRSA cases by type of specimens and wards.

All nonduplicate strains of S aureus isolated from clinical specimens in patients hospitalized for at least 24 hours during the survey period were included. Susceptibility tests were performed using national guidelines.16 Duplicate strains, defined as strains with the same antibiotic susceptibility pattern as a strain already counted for the same patient, were excluded.17,18 An MRSA case was defined as a patient with at least 1 clinical specimen positive for MRSA during the survey period. Strains of MRSA recovered from nares swabs (screening) were not included in the calculation of MRSA rates.

For each strain of S aureus included, the following data were recorded: date of sampling, type of ward, type of specimen, and antibiotic susceptibility pattern. From 1996 onwards, the number of patient-days and admissions was recorded for the calculation of MRSA incidence rates.

The data were computerized annually in each laboratory using Epi-info 6.04 (Centers for Disease Control and Prevention, Atlanta, Georgia) and then centralized and merged in a MySQL database (Sun Microsystems Inc, Santa Clara, California) using Perl software. The results were given as proportion (expressed as percentage) of MRSA among clinical isolates of S aureus and MRSA incidence rates per 1000 hospital days (HDs) and, for ACHs, per 100 admissions. Relative changes in MRSA rates were calculated as percentage over all the study period and per year. The susceptibility of MRSA strains to non–β-lactam antibiotics was also assessed.

ABHR SOLUTION USE

Following the launch in 2001 of the ABHR campaign, the annual ABHR solution use was recorded in liters per 1000 HDs using the data provided by the central pharmacy.

STATISTICAL ANALYSIS

The χ2 test for trend was used to analyze changes over time in the percentage of MRSA cases among clinical isolates of S aureus and of susceptibility to non–β-lactam antibiotics among MRSA strains, with R software (http://www.r-project.org). Poisson regression analysis was used to analyze changes over time in MRSA incidence rates, with SAS 8.02 software (SAS, Cary, North Carolina). Poisson confidence intervals were compared to analyze changes in MRSA incidence rates between the first and the last years of the survey using StatsDirect software (http://www.statsdirect.com). P < .05 was considered significant for all tests.

IMPLEMENTATION OF THE MRSA CONTROL PROGRAM IN AP-HP HOSPITALS

By 1995, 16 of the 23 ACHs and 5 of the 15 RLTCHs (P = .04) had implemented the program launched in 1993. Almost all the ACHs (19 of 23), but only 7 of the 15 RLTCHs, had done so in 1996 (P = .02). Reports sent from 1998 onwards by each hospital showed that notification of patients with MRSA infections or colonizations by laboratories had been implemented in all hospitals by 1998 and that active surveillance, targeting mainly ICUs, was implemented in almost all ACHs by 1998 and in all by 1999. Screening compliance was not recorded at central level but reached approximately 80% of the targeted patients in 12 ICUs of 5 hospitals that championed the initiative. By 2001, all ACHs, but a third of RLTCHs, had organized audits (eg, on hand hygiene), following local procedures and timing. Feedback information had been formalized by all hospitals by 2001.

USE OF ABHR SOLUTION

Following the ABHR campaign, use of ABHR solution increased regularly between 2000 and 2007 (Figure 1) from 2 L to 21 L per 1000 HDs but reached a higher level in ACHs than in RLTCHs (26 L and 10 L per 1000 HDs, respectively).

Place holder to copy figure label and caption
Figure 1.

Changes in the use of alcohol-based hand-rub solutions (in liters per 1000 HDs) from 1993 to 2007. ACHs indicates acute care hospitals; RLTCHs, rehabilitation and long-term care hospitals; and HDs, hospital days.

Graphic Jump Location
PROPORTION OF MRSA AMONG THE CLINICAL STRAINS OF S AUREUS

The proportion of MRSA among S aureus strains decreased from 39.4% in 1993 to 21.6% in 2007 in ACHs (relative change, −45%; P < .001), interrupted by a temporary rebound in 2000-2001 (Figure 2). The decrease was sharper in ICUs (from 55.1% to 22.4%; relative change, −59%; P < .001) and in surgical wards (from 38.7% to 21.7%; relative change, −44%; P < .001) than in medical wards (from 33.1% to 22.5%; relative change, −32%; P < .001) (Figure 3). The decline was significant and similar for 3 strata of ACHs (400-500, 800-1000, and >1000 beds). The decrease was also sharp in the strains isolated from blood cultures (from 45.3% to 24.2%; P < .001) and from pus and serous fluids (from 40.4% to 18.0%; P < .001).

Place holder to copy figure label and caption
Figure 2.

Change in methicillin-resistant Staphylococcus aureus (MRSA) rates from 1993 to 2007. Data are given as proportion (percentage) of MRSA in S aureus, MRSA incidence per 1000 hospital days, and MRSA rate per 100 admissions.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Change in the proportion (percentage) of MRSA strains in ICUs, surgery units, and medicine units from 1993 to 2007. ABHR indicates alcohol-based hand rub; ICUs intensive care units; and MRSA, methicillin-resistant Staphylococcus aureus. Error bars represent 95% confidence intervals.

Graphic Jump Location

In RLTCHs, the proportion of MRSA among S aureus strains remained high throughout the survey, ranging between 54% and 73%. As a result, the global decrease at AP-HP as a whole was less marked than in ACHs (from 41.0% in 1993 to 26.6% in 2007; relative change, −35%; P < .001).

INCIDENCE OF MRSA CASES

The incidence of MRSA cases decreased from 1.16 per 1000 HDs in 1996 to 0.57 in 2007 (relative change, −51%; P < .001) (Figure 2 and Figure 4). The decrease was sharper in ICUs (from 2.95 to 1.23 per 1000 HDs; relative change, −58%; P = .001) and in surgical wards (from 1.52 to 0.72 per 1000 HDs; −52%; P = .001) than in medical wards (from 0.70 to 0.48 per 1000 HDs; relative change, −31%; P = .04). When expressed per 100 admissions, the incidence of MRSA decreased in ACHs from 0.90 in 1996 to 0.44 in 2007 (P = .001).

Place holder to copy figure label and caption
Figure 4.

Change in MRSA incidence per 1000 HDs in ACHs and RLTCHs from 1996 to 2006. ABHR indicates alcohol-based hand rub; ACHs, acute care hospitals; HDs, hospital days; MRSA, methicillin-resistant Staphylococcus aureus; and RLTCHs, rehabilitation and long-term care hospitals. Error bars represent 95% confidence intervals.

Graphic Jump Location

In RLTCHs (Figure 4) the incidence rate initially increased from 0.49 to 0.94 per 1000 HDs between 1996 and 2001 (P = .001) and began to decrease only after 2001, down to 0.54 in 2007 (P = .001), ie, returning to the level observed in 1996. As a result, the global decrease in MRSA incidence in AP-HP as a whole was less marked than in ACHs, from 0.86 to 0.56 per 1000 HDs (relative change, −35%; P = .001).

TREND IN MRSA RATES BEFORE AND AFTER LAUNCHING THE ABHR CAMPAIGN

When introducing 2 periods (period 1, up to the ABHR campaign launch; period 2, after the campaign launch) in a multivariate model, the period was a significant variable of the decrease in MRSA incidence, but not the year, and interaction between the study period and year was established, justifying a separate analysis for each period. In ACHs, the MRSA rate decreased less sharply in period 1 (relative change, −2% per year) than in period 2 (relative change, −4.7% per year). The contrast was particularly apparent in medicine, where the percentage increased in period 1 (relative change, +2.3% per year) but decreased in period 2 (relative change, −6.2% per year). In surgery, the relative decrease was −1.8% per year in period 1 and −4.7% per year in period 2, but remained steady over both periods in ICUs.

SUSCEPTIBILITY PATTERN IN MRSA

Between 1993 and 2007, the susceptibility rates among MRSA strains significantly increased (P < .001) for gentamicin (from 12% to 95%), erythromycin (from 8% to 63%), and rifampicin (from 27% to 92%). In contrast, the susceptibility rates remained unchanged for fluoroquinolones (≤10%) and fusidic acid (>85%). The proportion of MRSA strains with decreased susceptibility to vancomycin (vancomycin intermediate-resistant S aureus, defined as vancomycin minimum inhibitory concentration >4 mg/L) remained below 1%.

An MRSA control program was launched in 1993 in the 38 hospitals of the AP-HP institution in response to the results of the first European MRSA comparative study conducted in 1990 showing high rates (approximately 35% of MRSA among the clinical isolates of S aureus) in France, Italy, and Spain, contrasting with low rates (<2%) in northern European countries.15 These results triggered the decision to take prompt action in our institution. Our MRSA control program was similar to, and largely based on, the guidelines published by national agencies that were available at that time2,4,19 and to which few changes have been made since.57 The program focused on a bundle of measures aimed at decreasing cross-transmission including single room placement, promotion of hand hygiene, active surveillance in high-risk patients, quick notification of cases, and feedback. Decolonization by mupirocin was not recommended due to the risk of resistance20 and was used scarcely. We did not close units where MRSA rates were particularly prevalent. Controlling antibiotic use was not attempted at the institution level during the study, and the overall use of antibiotics at AP-HP remained stable at approximately 450 defined daily doses per 1000 HDs.21 The MRSA control program was progressively implemented at AP-HP, more readily and completely in ACHs than in RLTCHs. The campaign launched halfway through the study to promote the use of ABHR solutions, whereas classic hand washing was advocated in the first phase of the study, led to a dramatic increase in ABHR solution use, sharper in ACHs than in RLTCHs.

The main result of the present study was the clear decrease in MRSA burden (−35%) between 1993 and 2007, whether expressed as a proportion of MRSA among clinical isolates of S aureus or the incidence of MRSA. The decline was steady and sharp in ICUs (−59%), where control measures have been readily implemented, and to a lesser extent in surgical wards (−44%) that are strongly connected with ICUs (many ICU patients are admitted for postsurgical complications and return to surgical wards when improving). In medical wards, where patients with MRSA infections or colonizations were scattered over a large number of units, likely hindering measure application, the decrease was less marked (−32%) and was delayed until the launch of the ABHR campaign in 2001. During the early years of the study, there was a trend to sharper decline in a subset of ACHs that led the initiative and generally applied more readily the program (results not shown). In RLTCHs, the decrease was delayed until 2001 and only counterbalanced the increase that initially occurred in 1993 to 2001, likely due to the difficulty to implement complex bundle measures and to hidden MRSA reservoirs in such setting. The decrease of MRSA in blood cultures (−47%) or pus and serous fluids (−55%) added clinical relevance to the results, based on all clinical specimens and not targeting specific infections.

The change in MRSA resistance patterns (increased susceptibility to gentamicin), already reported in France,9,22 was related to the rapid spread of new hospital clones with higher fitness that derived from older gentamicin-resistant clones,23,24 whereas clones producing the Panton-Valentine leukocidin (“community-acquired MRSA”), first identified in the early 2000s in French hospitals,25 represented less than 2% of our MRSA cases during the survey.26 Thus, virtually all our MRSA cases were hospital acquired, either locally or imported from other hospitals through previous stays or transfers, often within AP-HP, and were all recorded to assess the global MRSA burden in our institution. Vancomycin intermediate-resistant S aureus strains remained scarce as reported.27

The major limitation of our study is its observational design and lack of a control group. Indeed, the aim was to curb as quickly as possible the high MRSA rates prevailing in the early 1990s, and the study was conducted as a pragmatic intervention program in our whole institution. Consequently, we should be cautious in concluding that the statistically significant association between the MRSA decline and our control program implies a causal association. However, several facts support such an association. First, previous reports from French hospitals, including those of AP-HP, showed that the proportion of MRSA among S aureus strains increased steadily from approximately 15% in the 1970s to approximately 35% in the early 1990s,814,22 indicating that MRSA burden was not declining when our program was initiated. In fact, our program was launched in reaction to increasing MRSA rates. These reports actually provide “preintervention” measurements, which allow the present study to be considered as a “pre-post intervention” study.28,29 Unfortunately, the number of points of measurements (1 per year) was too low to allow a time series analysis.30 Second, the survey was carried out at the same time each year, avoiding seasonal differences, and used continuously the same definitions. The structure and recruitment of AP-HP hospitals did not change much either. Third, the efforts made to detect MRSA did not decline over time, since (1) volumes of clinical specimens did not decrease, allowing an overall inclusion of approximately 32 000 strains of S aureus, and (2) national guidelines published in 2000 introduced new sensitive tests to detect oxacillin resistance.16

Regression to the mean or local maturation effect are unlikely to explain the clear and sustained decline in MRSA rates observed in the present study that involved 38 hospitals covering a large geographical area.28,29,31 Interestingly, the decrease in MRSA burden at AP-HP during period 1 of the study (1993-2001) contrasts with a marked increase in MRSA rates that occurred between 1996 and 2000 in 23 hospitals scattered over the same part of France,32 but where MRSA control programs were introduced only in the early 2000s.33 Furthermore, the decrease measured during our period 2 (2001-2007) is consistent with the results of the European Antimicrobial Resistance Surveillance System (EARSS), which showed a decrease in MRSA prevalence in blood cultures between 2001 and 2006 in a set of hospitals scattered over France,3 after the introduction of the national MRSA control program.33 In contrast, EARSS data showed that MRSA rates were still on the increase during the years 2001 to 2006 in several countries with high MRSA burden, whereas they started to decline lately in several countries such as in the United Kingdom and Belgium.3

Effective control of MRSA in epidemic settings has been extensively demonstrated,2,5,7,19,31,3437 but the feasibility of controlling endemic situations with high MRSA rates has been questioned.3537 Our study demonstrates that this objective can be reached at the scale of a large medical institution. Partial control of MRSA was achieved in Belgian hospitals in the mid-1990s38 but was not maintained over time.3 Incidence of MRSA central line–associated bacteremia decreased in US ICUs between 1997 and 2007, likely due to bacteremia prevention, whereas the proportion of MRSA in S aureus strains actually increased.39

Modeling studies showed that only bundled measures confer efficacy in controlling MRSA,40 and all recommendations include such measures.57,34,36,37 The efficacy of single measures is difficult to evaluate separately,7,31,3436,41 particularly in our study owing to its design. However, it is noteworthy that MRSA rates declined first in ICUs where active surveillance (screening) has been already shown to improve patient contact isolation at AP-HP.4244 Screening is widely recommended7,3437 and allows early contact isolation and reduction in MRSA bacteremia in ICUs.45 We did not include screening results in MRSA rates because the variability in number of beds targeted would have introduce bias.46 Importantly, MRSA rates began to decline in medical wards and RLTCHs only during period 2 of the study, ie, after launching our ABHR campaign. Extensive use of ABHR solutions is known to increase hand hygiene compliance and MRSA control35,47,48 and ABHR use is now used as a crude marker of hand hygiene in France.49 Audits on hand hygiene organized at the local level likely played a role to improve compliance but were not recorded at central level owing to variability in methodology. At present, ABHR solutions are part of international actions in health care settings.50

Other measures likely played a role such as signaling procedures that helped to better identify patients with MRSA infections or colonizations19 and feedback that stimulated the efforts.36,51 Finally, a sustained leadership involved intensivists, bacteriologists, and infection control practitioners who championed the initiative, and a strong commitment of AP-HP administration provided an efficient incentive.

Although the decline in MRSA burden at AP-HP is very encouraging and led to generalize our initiative at the national level,33,49 the rates remained high in 2007 compared with those in northern Europe. Patients with MRSA infections or colonizations discharged from AP-HP still represent a source of secondary cases in household contacts.52 We should therefore maintain our efforts, particularly through antibiotic policy that is at present part of French national programs.49 Specific actions targeting serious infections such as catheter-related bacteremia would also contribute to hasten MRSA control.39

Correspondence: Vincent Jarlier, MD, PhD, Laboratoire de Bactériologie-Hygiène, Groupe Hospitalier Pitié-Salpêtrière, 47 Blvd de l’Hôpital, 75651 Paris CEDEX 13, France (vincent.jarlier@psl.aphp.fr).

Accepted for Publication: October 13, 2009.

Author Contributions: Dr Jarlier had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Jarlier, Marty, Andremont, Carlet, Gottot, Nicolas-Chanoine, and Aggoune. Acquisition of data: Jarlier, Trystram, Fournier, Carbonne, Marty, Andremont, Arlet, Buu-Hoi, Decré, Gutmann, Joly-Guillou, Legrand, Nicolas-Chanoine, Soussy, Wolf, and Brücker. Analysis and interpretation of data: Jarlier, Trystram, Brun-Buisson, Carbonne, Marty, Lucet, Brücker, and Régnier. Drafting of the manuscript: Jarlier, Fournier, and Gutmann. Critical revision of the manuscript for important intellectual content: Jarlier, Trystram, Brun-Buisson, Carbonne, Marty, Andremont, Arlet, Buu-Hoi, Carlet, Decré, Gottot, Joly-Guillou, Legrand, Nicolas-Chanoine, Soussy, Wolf, Lucet, Aggoune, Brücker, and Régnier. Statistical analysis: Trystram, Carbonne, and Marty. Administrative, technical, and material support: Brun-Buisson, Fournier, Carbonne, Marty, Andremont, Buu-Hoi, Gutmann, Joly-Guillou, Legrand, Soussy, Wolf, Lucet, Aggoune, and Brücker. Study supervision: Jarlier, Nicolas-Chanoine, and Régnier.

Financial Disclosure: None reported.

Additional Information: Dr Jarlier coordinated the survey and wrote the manuscript. Drs Trystram, Carbonne, and Marty were the successive data managers of the survey. Dr Brun-Buisson participated in the program design and headed the AP-HP infection control committee between 2000 and 2007. Drs Fournier, Lucet, and Brücker and Ms Aggoune were successively members of the infection control team at AP-HP central administration. Drs Andremont, Arlet, Buu-Hoi, Carlet, Decré, Gottot, Gutmann, Joly-Guillou, Legrand, Nicolas-Chanoine, Soussy, and Wolf participated in the program design. Drs Andremont, Gutmann, Nicolas-Chanoine, and Soussy participated in launching the bacteriological survey. Dr Régnier initiated the program and headed the AP-HP infection control committee between 1993 and 2000.

Additional Contributions: Stéphanie Depeigne, PharmD (central AP-HP pharmacy), provided data on alcohol-based hand-rub solutions and antibiotic use; Michelle Huang (intensive care nurse, AP-HP Central Infection Control Team) analyzed AP-HP hospital reports to the central administration; Yves Péan, MD, and Luis Stuardii, MD (Institut Mutualiste Monsouris), assisted in database design; and Pascal Astagneau, MD, PhD (Public Health Department, Université Pierre et Marie Curie, Paris), and Isabelle Arnaud, MSc (CCLIN Paris-Nord), assisted in statistical analysis.

Box Section Ref ID

Study and Group Information
AP-HP Hospitals, Heads of Laboratories of Bacteriology, Corresponding Members of the Collégiale de Bactériologie-Virologie-Hygiène des Hôpitaux Universitaires de l’Île-de-France, and Heads of the Infection Control Teams

The information is presented as follows: name of hospital (name of the head of laboratory/name[s] of the corresponding members/name of the head of the infection control team).

Hôpital Ambroise Paré–Sainte Perrine (J.-L. Gaillard/B. Heym/F. Espinasse), Hôpital Hôtel Dieu (A. Bouvet/S. Coignard/A. Casetta), Hôpital Necker–Enfants Malades–Vaugirard (P. Berche/A. Ferroni/J. R. Zahar), Hôpital Raymond Poincaré (J.-L. Gaillard/E. Ronco/C. Lawrence), Hôpital Cochin–Saint Vincent De Paul (C. Poyard/H. Poupet, J. Raymond/H. Blanchard), Hôpital HEGP–Corentin Celton (L. Gutmann/I. Podglagen/G. Kac, V. Moulin), Hôpital Beaujon (M.-H. Nicolas/F. Bert/D. Vanjak), Hôpital Bichat–Claude Bernard (A. Andremont/L. Armand-Lefevre/J.-C. Lucet), Hôpital Charles Richet (C. Abramowitz/L. Bensidhoum/N. Haber), Hôpital Jean Verdier (A. Collignon/I. Poilane/I. Durand), Hôpital Lariboisière–Fernand Widal (M.-J. Sanson-Le Pors/L. Raskine/J.-M. Guérin), Hôpital Louis Mourier (C. Branger/M. Eveillard/V. Fihman), Hôpital René Muret–Bigottini (A. Collignon/I. Durand/I. Durand), Hôpital Robert Debré (E. Bingen/C. Doit/C. Doit), Hôpital Saint-Louis (P. Lagrange/J.-L. Donnay/M. Rouveau), Hôpital Villemin–Paul Doumer (C. Cattoire/C. Cattoire/C. Cattoire), Hôpital Armand Trousseau (A. Gabarg-Chenon/H. Vu-Thien/B. Salauze), Hôpital Charles Foix–Jean Rostand (V. Jarlier/E. Cambau/A. Aubry), Hôpital Pitié–Salpêtrière (V. Jarlier/R. Bismuth, D. Trystram/J. Robert), Hôpital Rotschild (A. Gabarg-Chenon/H. Vu-Thien/B. Salauze), Hôpital Saint Antoine (J.-C. Petit/V. Lalande/F. Barbut), Hôpital Tenon (G. Arlet/G.Arlet/M. Denis), Hôpital Joffre–Dupuytren (C. Aussel/H. Nebbab-Lechani/N. Sabourin), Hôpital Antoine Beclère (D. Ingrand/C. Argentin/M. Guibert), Hôpital Bicêtre (P. Nordmann/C. Poy/N. Fortineau), Hôpital Emile Roux (C.-J. Soussy/A. Akpabie/A. Akpabie), Hôpital Georges Clémenceau (J.-L. Avril/F. Blonde-Cynober/L. Cukier), Hôpital Henri Mondor–Albert Chenevier (C.-J. Soussy/P. Legrand, L. Desforges, C. Dupeyron/E. Girou), Hôpital Paul Brousse (E. Dussaix/D. Mathieu/N. Kassis-Chikhani), Hôpital San Salvadour (V. Simha/M.-F. Lipens/V. Simha).

Klevens  RMEdwards  JRTenover  FCMcDonald  LCHoran  TGaynes  RNational Nosocomial Infections Surveillance System, Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992-2003. Clin Infect Dis 2006;42 (3) 389- 391
PubMed
Wenzel  RPNettleman  MDJones  RNPfaller  M Methicillin-resistant Staphylococcus aureus: implications for the 1990s and effective control measures. Am J Med 1991;91 (3B) 221S- 227S
PubMed
 The European Antimicrobial Resistance Surveillance System (EARSS) Web site. http://www.rivm.nl/earss/. Accessed June 17, 2009
Boyce  JM Methicillin-resistant Staphylococcus aureus: detection, epidemiology, and control measures. Infect Dis Clin North Am 1989;3 (4) 901- 913
PubMed
British Society for Antimicrobial Chemotherapy, Hospital Infection Society and the Infection Control Nurses Association, Revised guidelines for the control of epidemic methicillin-resistant Staphylococcus aureus infection in hospitals [published correction appears in J Hosp Infect. 1999;42(1):83]. J Hosp Infect 1998;39 (4) 253- 290
PubMed
Coia  JEDuckworth  GJEdwards  DI  et al. Joint Working Party of the British Society of Antimicrobial Chemotherapy; Hospital Infection Society; Infection Control Nurses Association, Guidelines for the control and prevention of methicillin-resistant Staphylococcus aureus (MRSA) in healthcare facilities [published correction appears in J Hosp Infect. 2006;64(1):97-98]. J Hosp Infect 2006;63 ((suppl 1)) S1- S44
PubMed
Muto  CAJernigan  JAOstrowsky  BE  et al. SHEA, SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infect Control Hosp Epidemiol 2003;24 (5) 362- 386
PubMed
Bismuth  RJarlier  VSinegre  MNguyen  JSednaoui  P Relation between bacterial sensitivity to antibiotics and the consumption of antibiotics, 2: study carried out on Staphylococcus aureus at the Pitié-Salpêtrière Hospital from 1975 to 1980 [in French]. Presse Med 1983;12 (2) 77- 81
PubMed
Lemaître  NSougakoff  WMasmoudi  AFievet  MHBismuth  RJarlier  V Characterization of gentamicin-susceptible strains of methicillin-resistant Staphylococcus aureus involved in nosocomial spread. J Clin Microbiol 1998;36 (1) 81- 85
PubMed
Duval  JSoussy  CJ Antibiothérapie: Bases Bactériologiques Pour l'Utilisation des Antibiotiques.  Paris, France Masson1990;
Réseau des Laboratoires du C.CLIN Sud-Ouest; Enquête Multicentrique, Résistance à la méticilline des Staphylococcus aureus dans les Hôpitaux du Sud Ouest de la France. Bulletin Epidémiologique Hebdomadaire 1995;1358- 59
Jarlier  V Bactéries multirésistantes dans les hôpitaux français: des premiers indicateurs au Réseau d’alerte d’investigation et de surveillance des infections nosocomiales (Raisin). Bulletin Epidémiologique Hebdomadaire 2004;32-33148- 150
Talon  DRBertrand  X Methicillin-resistant Staphylococcus aureus in geriatric patients: usefulness of screening in a chronic-care setting. Infect Control Hosp Epidemiol 2001;22 (8) 505- 509
PubMed
Marty  LJarlier  V Surveillance of multiresistant bacteria: justification, role of the laboratory, indicators, and recent French data. Pathol Biol (Paris) 1998;46 (4) 217- 226
PubMed
Voss  AMilatovic  DWallrauch-Schwarz  CRosdahl  VTBraveny  I Methicillin-resistant Staphylococcus aureus in Europe. Eur J Clin Microbiol Infect Dis 1994;13 (1) 50- 55
PubMed
Comité de l’Antibiogramme de la Société Française de Microbiologie, Les Recommandations du Comité de l'Antibiogramme (CA-SFM). 2007;http://www.sfm.asso.fr/publi/general.php?pa=1. Accessed June 17, 2009
Conseil Scientifique Observatoire National de l’Épidémiologie de la Résistance Bactérienne aux Antibiotiques, Recommandations méthodologiques pour la surveillance de la résistance aux antibiotiques dans les laboratoires de microbiologie. http://www.onerba.org/download/guide_onerba.pdf. Accessed June 17, 2009
Cornaglia  GHryniewicz  WJarlier  V  et al. ESCMID Study Group for Antimicrobial Resistance Surveillance, European recommendations for antimicrobial resistance surveillance. Clin Microbiol Infect 2004;10 (4) 349- 383
PubMed
 Revised guidelines for the control of epidemic methicillin-resistant Staphylococcus aureus: report of a combined working party of the Hospital Infection Society and British Society for Antimicrobial Chemotherapy. J Hosp Infect 1990;16 (4) 351- 377
PubMed
Miller  MADascal  APortnoy  JMendelson  J Development of mupirocin resistance among methicillin-resistant Staphylococcus aureus after widespread use of nasal mupirocin ointment. Infect Control Hosp Epidemiol 1996;17 (12) 811- 813
PubMed
WHO Collaborating Centre for Drug Statistics Methodology, The Anatomical Therapeutic Chemical Classification System/Defined Daily Doses (ATC/DDD). http://www.whocc.no/atc_ddd_methodology/purpose_of_the_atc_ddd_system/. Accessed June 17, 2009
Lelièvre  HLina  GJones  ME  et al.  Emergence and spread in French hospitals of methicillin-resistant Staphylococcus aureus with increasing susceptibility to gentamicin and other antibiotics. J Clin Microbiol 1999;37 (11) 3452- 3457
PubMed
Laurent  FLelièvre  HCornu  M  et al.  Fitness and competitive growth advantage of new gentamicin-susceptible MRSA clones spreading in French hospitals. J Antimicrob Chemother 2001;47 (3) 277- 283
PubMed
Robert  JBismuth  RLemaitre  NJarlier  V Gentamicin-susceptible or gentamicin-resistant methicillin-resistant Staphylococcus aureus: a case-case study. Infect Control Hosp Epidemiol 2006;27 (8) 879- 883
PubMed
Dufour  PGillet  YBes  M  et al.  Community-acquired methicillin-resistant Staphylococcus aureus infections in France: emergence of a single clone that produces Panton-Valentine leukocidin. Clin Infect Dis 2002;35 (7) 819- 824
PubMed
Robert  JEtienne  JBertrand  XONERBA (Observatoire National de l’Epidémiologie de la Résistance Bactérienne aux Antibiotiques), Methicillin-resistant Staphylococcus aureus producing Panton-Valentine leukocidin in a retrospective case series from 12 French hospital laboratories, 2000-2003. Clin Microbiol Infect 2005;11 (7) 585- 587
PubMed
Robert  JBismuth  RJarlier  V Decreased susceptibility to glycopeptides in methicillin-resistant Staphylococcus aureus: a 20 year study in a large French teaching hospital, 1983-2002. J Antimicrob Chemother 2006;57 (3) 506- 510
PubMed
Harris  ADBradham  DDBaumgarten  MZuckerman  HFink  JCPerencevich  EN The use and interpretation of quasi-experimental studies in infectious diseases. Clin Infect Dis 2004;38 (11) 1586- 1590
PubMed
Harris  ADLautenbach  EPerencevich  E A systematic review of quasi-experimental study designs in the fields of infection control and antibiotic resistance. Clin Infect Dis 2005;41 (1) 77- 81
PubMed
Monnet  DLLópez-Lozano  JMCampillos  PBurgos  AYagüe  AGonzalo  N Making sense of antimicrobial use and resistance surveillance data: application of ARIMA and transfer function models. Clin Microbiol Infect 2001;7 ((suppl 5)) 29- 36
PubMed
Cooper  BSStone  SPKibbler  CC  et al.  Systematic review of isolation policies in the hospital management of methicillin-resistant Staphylococcus aureus: a review of the literature with epidemiological and economic modelling. Health Technol Assess 2003;7 (39) 1- 194
PubMed
Albertini  MTBenoit  CBerardi  L  et al. Microbiology Surveillance Network of Northern France, Surveillance of methicillin-resistant Staphylococcus aureus (MRSA) and Enterobacteriaceae producing extended-spectrum beta-lactamase (ESBLE) in Northern France: a five-year multicentre incidence study. J Hosp Infect 2002;52 (2) 107- 113
PubMed
Astagneau  PCosta  YLegrand  PLucet  JMarty  LPrieur  B Maîtrise de la Diffusion des Bactéries Multirésistantes aux Antibiotiques.  Paris, France Ministère de l'Emploi et de la Solidarité Secrétariat d'Etat à la Santé et à l'Action Sociale Comité Technique National des Infections Nosocomiales1999;
Henderson  DK Managing methicillin-resistant staphylococci: a paradigm for preventing nosocomial transmission of resistant organisms. Am J Infect Control 2006;34 (5) ((suppl 1)) S46- S54, S64-S73
PubMed
Harbarth  S Control of endemic methicillin-resistant Staphylococcus aureus—recent advances and future challenges. Clin Microbiol Infect 2006;12 (12) 1154- 1162
PubMed
Marshall  CWesselingh  SMcDonald  MSpelman  D Control of endemic MRSA—what is the evidence? a personal view. J Hosp Infect 2004;56 (4) 253- 268
PubMed
Boyce  JMHavill  NLKohan  CDumigan  DGLigi  CE Do infection control measures work for methicillin-resistant Staphylococcus aureus? Infect Control Hosp Epidemiol 2004;25 (5) 395- 401
PubMed
Struelens  MJRonveaux  OJans  BMertens  RGroupement pour le Dépistage, l'Etude et la Prévention des Infections Hospitalières, Methicillin-resistant Staphylococcus aureus epidemiology and control in Belgian hospitals, 1991 to 1995. Infect Control Hosp Epidemiol 1996;17 (8) 503- 508
PubMed
Burton  DCEdwards  JRHoran  TCJernigan  JAFridkin  SK Methicillin-resistant Staphylococcus aureus central line-associated bloodstream infections in US intensive care units, 1997-2007. JAMA 2009;301 (7) 727- 736
PubMed
Bootsma  MCJDiekmann  OBonten  MJM Controlling methicillin-resistant Staphylococcus aureus: a quantifying the effects of interventions and rapid diagnostic testing. Proc Natl Acad Sci U S A 2006;103 (14) 5620- 5625
PubMed
Humphreys  H National guidelines for the control and prevention of methicillin-resistant Staphylococcus aureus—what do they tell us? Clin Microbiol Infect 2007;13 (9) 846- 853
PubMed
Girou  EPujade  GLegrand  PCizeau  FBrun-Buisson  C Selective screening of carriers for control of methicillin-resistant Staphylococcus aureus (MRSA) in high-risk hospital areas with a high level of endemic MRSA. Clin Infect Dis 1998;27 (3) 543- 550
PubMed
Lucet  JCChevret  SDurand-Zaleski  IChastang  CRégnier  BMulticenter Study Group, Prevalence and risk factors for carriage of methicillin-resistant Staphylococcus aureus at admission to the intensive care unit: results of a multicenter study. Arch Intern Med 2003;163 (2) 181- 188
PubMed
Lucet  JCPaoletti  XLolom  I  et al.  Successful long-term program for controlling methicillin-resistant Staphylococcus aureus in intensive care units. Intensive Care Med 2005;31 (8) 1051- 1057
PubMed
Huang  SSYokoe  DSHinrichsen  VL  et al.  Impact of routine intensive care unit surveillance cultures and resultant barrier precautions on hospital-wide methicillin-resistant Staphylococcus aureus bacteremia. Clin Infect Dis 2006;43 (8) 971- 978
PubMed
L'Hériteau  FAlberti  CCohen  YTroché  GMoine  PTimsit  JF Nosocomial infection and multidrug-resistant bacteria surveillance in intensive care units: a survey in France. Infect Control Hosp Epidemiol 2005;26 (1) 13- 20
PubMed
Pittet  DHugonnet  SHarbarth  S  et al.  Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Lancet 2000;356 (9238) 1307- 1312
PubMed
Harbarth  SPittet  DGrady  L  et al.  Interventional study to evaluate the impact of an alcohol-based hand gel in improving hand hygiene compliance. Pediatr Infect Dis J 2002;21 (6) 489- 495
PubMed
Carlet  JAstagneau  PBrun-Buisson  C  et al. French National Program for Prevention of Healthcare-Associated Infections and Antimicrobial Resistance, French National Program for Prevention of Healthcare-Associated Infections and Antimicrobial Resistance, 1992-2008: positive trends, but perseverance needed. Infect Control Hosp Epidemiol 2009;30 (8) 737- 745
PubMed
World Health Organization, WHO patient safety. http://www.who.int/patientsafety/en. Accessed June 17, 2009
Nettleman  MDTrilla  AFredrickson  MPfaller  M Assigning responsibility: using feedback to achieve sustained control of methicillin-resistant Staphylococcus aureus. Am J Med 1991;91 (3B) 228S- 232S
PubMed
Lucet  JCPaoletti  XDemontpion  C  et al. Staphylococcus aureus Resistant a la Meticilline en Hospitalisation A Domicile (SARM HAD) Study Group, Carriage of methicillin-resistant Staphylococcus aureus in home care setting: prevalence, duration, and transmission to household members. Arch Intern Med 2009;169 (15) 1372- 1378
PubMed

Figures

Place holder to copy figure label and caption
Figure 1.

Changes in the use of alcohol-based hand-rub solutions (in liters per 1000 HDs) from 1993 to 2007. ACHs indicates acute care hospitals; RLTCHs, rehabilitation and long-term care hospitals; and HDs, hospital days.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Change in methicillin-resistant Staphylococcus aureus (MRSA) rates from 1993 to 2007. Data are given as proportion (percentage) of MRSA in S aureus, MRSA incidence per 1000 hospital days, and MRSA rate per 100 admissions.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Change in the proportion (percentage) of MRSA strains in ICUs, surgery units, and medicine units from 1993 to 2007. ABHR indicates alcohol-based hand rub; ICUs intensive care units; and MRSA, methicillin-resistant Staphylococcus aureus. Error bars represent 95% confidence intervals.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 4.

Change in MRSA incidence per 1000 HDs in ACHs and RLTCHs from 1996 to 2006. ABHR indicates alcohol-based hand rub; ACHs, acute care hospitals; HDs, hospital days; MRSA, methicillin-resistant Staphylococcus aureus; and RLTCHs, rehabilitation and long-term care hospitals. Error bars represent 95% confidence intervals.

Graphic Jump Location

Tables

References

Klevens  RMEdwards  JRTenover  FCMcDonald  LCHoran  TGaynes  RNational Nosocomial Infections Surveillance System, Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992-2003. Clin Infect Dis 2006;42 (3) 389- 391
PubMed
Wenzel  RPNettleman  MDJones  RNPfaller  M Methicillin-resistant Staphylococcus aureus: implications for the 1990s and effective control measures. Am J Med 1991;91 (3B) 221S- 227S
PubMed
 The European Antimicrobial Resistance Surveillance System (EARSS) Web site. http://www.rivm.nl/earss/. Accessed June 17, 2009
Boyce  JM Methicillin-resistant Staphylococcus aureus: detection, epidemiology, and control measures. Infect Dis Clin North Am 1989;3 (4) 901- 913
PubMed
British Society for Antimicrobial Chemotherapy, Hospital Infection Society and the Infection Control Nurses Association, Revised guidelines for the control of epidemic methicillin-resistant Staphylococcus aureus infection in hospitals [published correction appears in J Hosp Infect. 1999;42(1):83]. J Hosp Infect 1998;39 (4) 253- 290
PubMed
Coia  JEDuckworth  GJEdwards  DI  et al. Joint Working Party of the British Society of Antimicrobial Chemotherapy; Hospital Infection Society; Infection Control Nurses Association, Guidelines for the control and prevention of methicillin-resistant Staphylococcus aureus (MRSA) in healthcare facilities [published correction appears in J Hosp Infect. 2006;64(1):97-98]. J Hosp Infect 2006;63 ((suppl 1)) S1- S44
PubMed
Muto  CAJernigan  JAOstrowsky  BE  et al. SHEA, SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infect Control Hosp Epidemiol 2003;24 (5) 362- 386
PubMed
Bismuth  RJarlier  VSinegre  MNguyen  JSednaoui  P Relation between bacterial sensitivity to antibiotics and the consumption of antibiotics, 2: study carried out on Staphylococcus aureus at the Pitié-Salpêtrière Hospital from 1975 to 1980 [in French]. Presse Med 1983;12 (2) 77- 81
PubMed
Lemaître  NSougakoff  WMasmoudi  AFievet  MHBismuth  RJarlier  V Characterization of gentamicin-susceptible strains of methicillin-resistant Staphylococcus aureus involved in nosocomial spread. J Clin Microbiol 1998;36 (1) 81- 85
PubMed
Duval  JSoussy  CJ Antibiothérapie: Bases Bactériologiques Pour l'Utilisation des Antibiotiques.  Paris, France Masson1990;
Réseau des Laboratoires du C.CLIN Sud-Ouest; Enquête Multicentrique, Résistance à la méticilline des Staphylococcus aureus dans les Hôpitaux du Sud Ouest de la France. Bulletin Epidémiologique Hebdomadaire 1995;1358- 59
Jarlier  V Bactéries multirésistantes dans les hôpitaux français: des premiers indicateurs au Réseau d’alerte d’investigation et de surveillance des infections nosocomiales (Raisin). Bulletin Epidémiologique Hebdomadaire 2004;32-33148- 150
Talon  DRBertrand  X Methicillin-resistant Staphylococcus aureus in geriatric patients: usefulness of screening in a chronic-care setting. Infect Control Hosp Epidemiol 2001;22 (8) 505- 509
PubMed
Marty  LJarlier  V Surveillance of multiresistant bacteria: justification, role of the laboratory, indicators, and recent French data. Pathol Biol (Paris) 1998;46 (4) 217- 226
PubMed
Voss  AMilatovic  DWallrauch-Schwarz  CRosdahl  VTBraveny  I Methicillin-resistant Staphylococcus aureus in Europe. Eur J Clin Microbiol Infect Dis 1994;13 (1) 50- 55
PubMed
Comité de l’Antibiogramme de la Société Française de Microbiologie, Les Recommandations du Comité de l'Antibiogramme (CA-SFM). 2007;http://www.sfm.asso.fr/publi/general.php?pa=1. Accessed June 17, 2009
Conseil Scientifique Observatoire National de l’Épidémiologie de la Résistance Bactérienne aux Antibiotiques, Recommandations méthodologiques pour la surveillance de la résistance aux antibiotiques dans les laboratoires de microbiologie. http://www.onerba.org/download/guide_onerba.pdf. Accessed June 17, 2009
Cornaglia  GHryniewicz  WJarlier  V  et al. ESCMID Study Group for Antimicrobial Resistance Surveillance, European recommendations for antimicrobial resistance surveillance. Clin Microbiol Infect 2004;10 (4) 349- 383
PubMed
 Revised guidelines for the control of epidemic methicillin-resistant Staphylococcus aureus: report of a combined working party of the Hospital Infection Society and British Society for Antimicrobial Chemotherapy. J Hosp Infect 1990;16 (4) 351- 377
PubMed
Miller  MADascal  APortnoy  JMendelson  J Development of mupirocin resistance among methicillin-resistant Staphylococcus aureus after widespread use of nasal mupirocin ointment. Infect Control Hosp Epidemiol 1996;17 (12) 811- 813
PubMed
WHO Collaborating Centre for Drug Statistics Methodology, The Anatomical Therapeutic Chemical Classification System/Defined Daily Doses (ATC/DDD). http://www.whocc.no/atc_ddd_methodology/purpose_of_the_atc_ddd_system/. Accessed June 17, 2009
Lelièvre  HLina  GJones  ME  et al.  Emergence and spread in French hospitals of methicillin-resistant Staphylococcus aureus with increasing susceptibility to gentamicin and other antibiotics. J Clin Microbiol 1999;37 (11) 3452- 3457
PubMed
Laurent  FLelièvre  HCornu  M  et al.  Fitness and competitive growth advantage of new gentamicin-susceptible MRSA clones spreading in French hospitals. J Antimicrob Chemother 2001;47 (3) 277- 283
PubMed
Robert  JBismuth  RLemaitre  NJarlier  V Gentamicin-susceptible or gentamicin-resistant methicillin-resistant Staphylococcus aureus: a case-case study. Infect Control Hosp Epidemiol 2006;27 (8) 879- 883
PubMed
Dufour  PGillet  YBes  M  et al.  Community-acquired methicillin-resistant Staphylococcus aureus infections in France: emergence of a single clone that produces Panton-Valentine leukocidin. Clin Infect Dis 2002;35 (7) 819- 824
PubMed
Robert  JEtienne  JBertrand  XONERBA (Observatoire National de l’Epidémiologie de la Résistance Bactérienne aux Antibiotiques), Methicillin-resistant Staphylococcus aureus producing Panton-Valentine leukocidin in a retrospective case series from 12 French hospital laboratories, 2000-2003. Clin Microbiol Infect 2005;11 (7) 585- 587
PubMed
Robert  JBismuth  RJarlier  V Decreased susceptibility to glycopeptides in methicillin-resistant Staphylococcus aureus: a 20 year study in a large French teaching hospital, 1983-2002. J Antimicrob Chemother 2006;57 (3) 506- 510
PubMed
Harris  ADBradham  DDBaumgarten  MZuckerman  HFink  JCPerencevich  EN The use and interpretation of quasi-experimental studies in infectious diseases. Clin Infect Dis 2004;38 (11) 1586- 1590
PubMed
Harris  ADLautenbach  EPerencevich  E A systematic review of quasi-experimental study designs in the fields of infection control and antibiotic resistance. Clin Infect Dis 2005;41 (1) 77- 81
PubMed
Monnet  DLLópez-Lozano  JMCampillos  PBurgos  AYagüe  AGonzalo  N Making sense of antimicrobial use and resistance surveillance data: application of ARIMA and transfer function models. Clin Microbiol Infect 2001;7 ((suppl 5)) 29- 36
PubMed
Cooper  BSStone  SPKibbler  CC  et al.  Systematic review of isolation policies in the hospital management of methicillin-resistant Staphylococcus aureus: a review of the literature with epidemiological and economic modelling. Health Technol Assess 2003;7 (39) 1- 194
PubMed
Albertini  MTBenoit  CBerardi  L  et al. Microbiology Surveillance Network of Northern France, Surveillance of methicillin-resistant Staphylococcus aureus (MRSA) and Enterobacteriaceae producing extended-spectrum beta-lactamase (ESBLE) in Northern France: a five-year multicentre incidence study. J Hosp Infect 2002;52 (2) 107- 113
PubMed
Astagneau  PCosta  YLegrand  PLucet  JMarty  LPrieur  B Maîtrise de la Diffusion des Bactéries Multirésistantes aux Antibiotiques.  Paris, France Ministère de l'Emploi et de la Solidarité Secrétariat d'Etat à la Santé et à l'Action Sociale Comité Technique National des Infections Nosocomiales1999;
Henderson  DK Managing methicillin-resistant staphylococci: a paradigm for preventing nosocomial transmission of resistant organisms. Am J Infect Control 2006;34 (5) ((suppl 1)) S46- S54, S64-S73
PubMed
Harbarth  S Control of endemic methicillin-resistant Staphylococcus aureus—recent advances and future challenges. Clin Microbiol Infect 2006;12 (12) 1154- 1162
PubMed
Marshall  CWesselingh  SMcDonald  MSpelman  D Control of endemic MRSA—what is the evidence? a personal view. J Hosp Infect 2004;56 (4) 253- 268
PubMed
Boyce  JMHavill  NLKohan  CDumigan  DGLigi  CE Do infection control measures work for methicillin-resistant Staphylococcus aureus? Infect Control Hosp Epidemiol 2004;25 (5) 395- 401
PubMed
Struelens  MJRonveaux  OJans  BMertens  RGroupement pour le Dépistage, l'Etude et la Prévention des Infections Hospitalières, Methicillin-resistant Staphylococcus aureus epidemiology and control in Belgian hospitals, 1991 to 1995. Infect Control Hosp Epidemiol 1996;17 (8) 503- 508
PubMed
Burton  DCEdwards  JRHoran  TCJernigan  JAFridkin  SK Methicillin-resistant Staphylococcus aureus central line-associated bloodstream infections in US intensive care units, 1997-2007. JAMA 2009;301 (7) 727- 736
PubMed
Bootsma  MCJDiekmann  OBonten  MJM Controlling methicillin-resistant Staphylococcus aureus: a quantifying the effects of interventions and rapid diagnostic testing. Proc Natl Acad Sci U S A 2006;103 (14) 5620- 5625
PubMed
Humphreys  H National guidelines for the control and prevention of methicillin-resistant Staphylococcus aureus—what do they tell us? Clin Microbiol Infect 2007;13 (9) 846- 853
PubMed
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