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Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci co-colonization (1).



We assessed the prevalence, risk factors, and clinical outcomes of patients co-colonized with vancomycin-resistant enterococci enterococci

bacteria in the genus Enterococcus.
 (VRE VRE

vancomycin-resistant enterococcus.

VRE Vancomycin-resistent enterococcus, see there
) and methicillin-resistant Staphylococcus aureus methicillin-resistant Staphylococcus aureus Methicillin-aminoglycoside resistant Staphylococcus aureus, MRSA An organism with multiple antibiotic resistances–eg, aminoglycosides, chloramphenicol, clindamycin, erythromycin, rifampin, tetracycline,  (MRSA MRSA Methicillin-resistant Staphylococcus aureus. See MARSA. ) upon admission to the medical and surgical intensive care units (ICUs) of a tertiary-care facility between January 1, 2002, and December 31, 2003. Co-colonization was defined as a VRE-positive perirectal surveillance culture with an MRSA-positive anterior nares The Anterior Nares are the external (or "proper") portion of the nostrils (nose).[1] Common Infections (MRSA)
Commonly infected by Staphylococcus aureus
 surveillance culture collected concurrently. Among 2,440 patients, 65 (2.7%) were co-colonized. Independent risk factors included age (odds ratio [OR] 1.03, 95% confidence interval confidence interval,
n a statistical device used to determine the range within which an acceptable datum would fall. Confidence intervals are usually expressed in percentages, typically 95% or 99%.
 [CI] 1.01-1.05), admission to the medical ICU ICU intensive care unit.

ICU
abbr.
intensive care unit



ICU

see intensive care unit.

ICU 
 (OR 4.38, 95% CI 2.46-7.81), male sex (OR 1.93, 95% CI 1.14-3.30), and receiving antimicrobial drugs on a previous admission within 1 year (OR 3.06, 95% CI 1.85-5.07). None of the co-colonized patients would have been identified with clinical cultures alone. We report a high prevalence of VRE/MRSA co-colonization upon admission to ICUs at a tertiary-care hospital.

**********

Methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant enterococci (VRE) cause nosocomial infections Nosocomial infections
Infections that were not present before the patient came to a hospital, but were acquired by a patient while in the hospital.

Mentioned in: Enterobacterial Infections, Staphylococcal Infections
 and are associated with increased rates of illness and death (1,2). Both organisms are now endemic in many healthcare institutions, particularly in intensive care units (ICUs) (3). Vancomycin vancomycin (văn'kōmī`sĭn), antibiotic resembling penicillin in the way it acts. It is derived from the bacterium Streptomyces orientalis, which was isolated from soil of India and Indonesia.  is commonly used to treat infections caused by MRSA; however, recent emergence of S. aureus The aureus (pl. aurei) was a gold coin of ancient Rome valued at 25 silver denarii. The aureus was regularly issued from the 1st century BC to the beginning of the 4th century AD, when it was replaced by the solidus.  infections with high-level resistance to vancomycin call into question the future effectiveness of vancomycin for these nosocomial infections (4). All known vancomycin-resistant S. aureus (VRSA VRSA Vancomycin-resistant Staphylococcus aureus. Cf Vancomycin-resistant enterococcus. ) isolates reported thus far have possessed the vanA gene, which confers resistance to vancomycin and is believed to have been acquired when an MRSA isolate conjugated conjugated
adj.
Conjugate.


estrogens, conjugated Warning - Hazardous drug!

C.E.S.
 with a co-colonizing VRE isolate (5-10). Thus, patients simultaneously co-colonized with MRSA and VRE are likely at increased risk for colonization or infection by VRSA.

Patients in the 1CU and other critically ill patients are at high risk for co-colonization with MRSA and VRE and, possibly, VRSA, since both organisms are endemic and associated with increased illness severity (11,12). Despite the high risk, epidemiologic risk factors associated with co-colonization by MRSA and VRE in patients admitted to ICUs have not been described. In addition, previous studies in this population have been limited by the use of clinical cultures as markers for colonization, which underestimate the true proportion of patients colonized Colonized
This occurs when a microorganism is found on or in a person without causing a disease.

Mentioned in: Isolation
 with these resistant organisms (13-15).

To our knowledge, this study is the first to assess independent risk factors and outcomes for patients co-colonized with VRE and MRSA. The aim of this study was to estimate the prevalence, risk factors, and clinical outcomes of patients who are co-colonized by VRE and MRSA upon admission to the medical and surgical ICUs of a tertiary-care facility.

Methods

Study Design and Patient Population

This study was approved by the institutional review board of the University of Maryland, Baltimore University of Maryland, Baltimore, (also known as UMB) was founded in 1807. It is one of the oldest universities in the United States and comprises some of the oldest professional schools in the nation and world. . This study utilized a prospective cohort of adult patients admitted to the medical ICU (MICU MICU Mobile intensive care unit Emergency medicine A vehicle, usually a specially-designed minivan or truck with the capacity for providing emergency care and life support to the severely injured or ill at the scene of an accident or natural disaster and ) and surgical ICU (SICU SICU Surgical intensive care unit. See ICU. ) of the University of Maryland University of Maryland can refer to:
  • University of Maryland, College Park, a research-extensive and flagship university; when the term "University of Maryland" is used without any qualification, it generally refers to this school
 Medical Center (UMMC UMMC University of Maryland Medical Center
UMMC University of Michigan Medical Center
UMMC Unspecified Minor Military Construction
) between January 1, 2002, and December 31, 2003. UMMC is a tertiary-care facility in Baltimore, Maryland "Baltimore" redirects here. For the surrounding county, see Baltimore County, Maryland. For other uses, see Baltimore (disambiguation).
Baltimore is an independent city located in the state of Maryland in the United States.
. The MICU is a 10-bed, private room unit providing care to patients who have acute or potentially life-threatening medical conditions See carpal tunnel syndrome, computer vision syndrome, dry eyes and deep vein thrombosis.  including hematologic hematological, hematologic

pertaining to or emanating from blood cells.


hematological tests
total and differential white cell counts, hematocrit estimation, erythrocyte count.
 and other malignancies. The SICU is a 19-bed, private room unit providing care to adult patients with solid organ transplantation The transfer of organs such as the kidneys, heart, or liver from one body to another.

The transplantation of human organs has become a common medical procedure. Typical organs transplanted are the kidneys, heart, liver, pancreas, cornea, skin, bones, and lungs.
 and abdominal, genitourinary genitourinary /gen·i·to·uri·nary/ (jen?i-to-u´ri-nar-e) pertaining to the genital and urinary organs.

gen·i·to·u·ri·nar·y
adj. Abbr.
, orthopedic, and otolaryngologic surgery.

During the study period, routine surveillance cultures of the anterior nares for MRSA and perirectal area for VRE were obtained from patients within 48 hours of admission to both ICUs for infection control purposes. Cultures were obtained from an average of 80% of admitted patients. Patients from whom both cultures were not obtained upon ICU admission or had an ICU length of stay <5 hours were excluded. Patients may have had multiple admissions during the study period, and all eligible admissions were included in this analysis.

Data Collection and Variables

All data were abstracted from the UMMC central data repository See repository.  that contains the patients' electronic medical records. The validity of these data was assessed by randomly sampling 10% of the patients' electronic data records and comparing them to the original paper medical records. The positive and negative predictive values of this assessment exceeded 99% for both validity measures, which was similar to values seen in previous studies with this same data source (16-19).

Co-colonization by VRE and MRSA upon ICU admission was defined as a positive surveillance culture of the perirectal area for VRE and a positive surveillance culture of the anterior nares for MRSA within 48 hours of admission to either the MICU or SICU. All coexisting conditions were defined by using International Classification of Diseases, 9th Revision and the Charlson Comorbidity Index (20).

Laboratory Methods

All media and reagents were from BD Biosciences (San Jose San Jose, city, United States
San Jose (sănəzā`, săn hōzā`), city (1990 pop. 782,248), seat of Santa Clara co., W central Calif.; founded 1777, inc. 1850.
, CA, USA) unless otherwise noted. S. aureus was isolated from both anterior nares and perirectal cultures. Nares swabs were plated on tryptic tryp·tic
adj.
Relating to or resulting from trypsin.



tryptic

relating to or resulting from digestion by trypsin.
 soy agar with 5% sheep blood to isolate S. aureus. Plates were examined at 24 and 48 hours for creamy, golden [beta]-hemolytic colonies typical of S. aureus. Perirectal swabs were plated on both tryptic soy agar with 5% sheep blood and phenylethyl alcohol phen·yl·eth·yl alcohol
n.
An antibacterial agent that is the natural constituent of certain volatile oils.
 agar (Remel, Lenexa, KS, USA) and cultured in Baird Staphylococcus staphylococcus (stăf'ələkŏk`əs), any of the pathogenic bacteria, parasitic to humans, that belong to the genus Staphylococcus. The spherical bacterial cells (cocci) typically occur in irregular clusters [Gr.  Enrichment broth (Merck, Darmstadt, Germany). Presumptive S. aureus colonies were confirmed by positive catalase catalase /cat·a·lase/ (kat´ah-las) a hemoprotein enzyme that catalyzes the decomposition of hydrogen peroxide to water and oxygen, protecting cells.  and Murex mu·rex  
n. pl. mu·ri·ces or mu·rex·es
Any of various marine gastropods of the genus Murex common in tropical seas and having rough spiny shells, especially M. trunculus, the source of Tyrian purple.
 Staphaurex (Remel) reactions. MRSA were identified by growth on Mueller Hinton agar with 4% NaCl and 6 [micro]g/mL oxacillin oxacillin /ox·a·cil·lin/ (ok?sah-sil´in) a semisynthetic penicillinase-resistant penicillin used as the sodium salt in infections due to penicillin-resistant, gram-positive organisms. .

Enterococci were isolated by plating perirectal swabs on Columbia Modified CNA (Certified NetWare Administrator) See Novell certification.  agar and examined at 24 and 48 hours. Presumptive enterococci colonies that were gram-positive cocci cocci /coc·ci/ (kok´si) plural of coccus.

cocci

[L.] plural of coccus.
, catalase negative, and pyrrolidonyl-[beta]-naphthylamide positive were plated on vancomycin screening agar and motility motility /mo·til·i·ty/ (mo-til´ite) the ability to move spontaneously.mo´tile
Motility
Motility is spontaneous movement.
 agar. Vancomycin-resistant, nonmotile enterococci were identified as VRE.

Statistical Analyses

Three risk factor analyses were conducted: 1) VRE/MRSA co-colonized patients were compared to all other ICU patients, 2) patients colonized with VRE alone were compared to patients not colonized with VRE, and 3) patients colonized with MRSA alone were compared to patients not colonized with MRSA. Patients co-colonized with MRSA or VRE were excluded for analyses 2 and 3 above that compared solitary VRE or MRSA colonization to noncolonized patients.

Student t, chi-square, Fisher exact, and Wilcoxon rank sum tests were used for descriptive analyses to assess bivariable differences between groups. All variables that were significant ([alpha] = 0.1) in the bivariable analyses were included in the initial (full) multivariable logistic regression In statistics, logistic regression is a regression model for binomially distributed response/dependent variables. It is useful for modeling the probability of an event occurring as a function of other factors.  model. In each of the multivariable analyses performed, variables not significantly associated ([alpha] = 0.05) with the outcome (VRE/MRSA co-colonization and VRE or MRSA solitary colonization upon admission to the ICU) were removed from the model. Each of the removed variables was then reinserted into the model to assess if its presence altered the regression coefficient Regression coefficient

Term yielded by regression analysis that indicates the sensitivity of the dependent variable to a particular independent variable. See: Parameter.


regression coefficient 
 by [greater than or equal to] 20%. If so, this risk factor was included in the final model. The resulting multivariable logistic regression model was considered the final model and was used to calculate odds ratios and 95% confidence intervals for the remaining risk factors.

Differences in patients' clinical outcomes after assessing colonization status were also assessed. These variables included length of stay after the ICU admission culture, subsequent positive clinical cultures for VRE or MRSA, in-hospital death rate, and readmission readmission Managed care The admission of a Pt to a health care facility for a condition–eg, stroke, MI, GI bleeding, hip fracture, cancer surgery, shortly after discharge. See nth admission. Cf Admission, Discharge.  to the index hospital or transfer to another healthcare facility. Subsequent positive clinical cultures were limited to sterile sites, and thus only blood, cerebrospinal fluid cerebrospinal fluid (CSF)

Clear, colourless liquid that surrounds the brain and spinal cord and fills the spaces in them. It helps support the brain, acts as a lubricant, maintains pressure in the skull, and cushions shocks.
, or urine cultures were considered.

Results

During the 2-year cohort period (January 1, 2002-December 31, 2003), 3,090 patients were admitted to the MICU or SICU for a >5-hour stay. Of these, 2,440 patients (79.0%) had both anterior nares and perirectal admission cultures collected. Sixty-five patients (2.7%) were co-colonized with VRE and MRSA, 247 patients (10.1%) were colonized with VRE alone, and 175 patients (7.2%) were colonized with MRSA alone. Of the 57 MRSA/VRE co-colonized patients with perirectal samples available for additional analysis, 23 patients (40.4%) were perirectally colonized with MRSA in addition to perirectal VRE and MRSA nasal colonization. Results of the bivariable analyses for VRE/MRSA co-colonization are displayed in Table 1. Because of space constraints, bivariable results for colonization by MRSA or VRE alone are not shown. These results suggest that patients colonized with VRE, MRSA, or both were significantly more likely to have been admitted to the MICU, have had previous hospital admissions, and have antimicrobial exposures within 1 year of current admission (p<0.05 for all). Among co-colonized patients, 58% had been admitted to the index hospital in the previous year, and 51% had received antimicrobial drugs during an admission in the previous year. In addition, [approximately equal to] 48% of MRSA/VRE co-colonized patients had a previous positive culture (clinical or surveillance) for MRSA before the study period, and [approximately equal to] 28% had a previous positive culture for VRE.

Independent risk factors identified with logistic regression for the different colonization states (co-colonization, VRE only, or MRSA only) were markedly different (Table 2). Table 3 displays clinical outcomes of VRE/MRSA co-colonized patients. Approximately 25% percent of co-colonized patients died during the current admission; however, mortality was not significantly higher compared to non-co-colonized patients (p = 0.15). Three percent of co-colonized patients had MRSA-positive clinical cultures, and 3% of co-colonized patients had VRE-positive clinical cultures on the current or subsequent admissions (within 6 months). None of the co-colonized patients had clinical cultures positive for both organisms. Thirty-two percent of VRE/MRSA co-colonized patients were transferred to another hospital upon discharge from the index hospital compared with 15% of non-co-colonized patients (p<0.01).

Discussion

Increasing VRSA prevalence in the healthcare setting could result in considerable illness and death (21). To our knowledge, we present the first estimates of the prevalence, risk factors, and clinical outcomes of patients with VRE and MRSA co-colonization. As has been previously reported, co-colonization with VRE and MRSA has always preceded VRSA colonization or infection, and patients admitted to ICUs are likely a high-risk population (11-13,15). We show that among patients who had admission cultures taken, 4.6% admitted to the MICU and 1.2% admitted to the SICU of a tertiary-care facility during a 2-year period were co-colonized with MRSA and VRE, with an overall co-colonization proportion of 3% in both ICUs together. In addition, the observation that [approximately equal to] 40% of MRSA/VRE co-colonized patients were perirectally colonized with both organisms suggests the potential risk for the exchange of genetic material, which could result in the emergence of VRSA.

None of the 65 VRE/MRSA-co-colonized patients had positive clinical cultures for both VRE and MRSA on current or subsequent admissions to the index hospital. Thus, none would have been identified as co-colonized without the active surveillance culturing program in place at our institution. As has been suggested by previously reported cases of VRSA, early identification of these patients is recommended to minimize antimicrobial selective pressure and enhance infection control efforts to reduce the potential for patient-to-patient transmission (5,7).

In this study, <25% of co-colonized patients died, and nearly 35% were discharged to other hospitals or rehabilitation facilities, where the risk of transmitting these organisms to other patients is substantial. Considering the potential for colonization, infection, and transmission of VRSA, treating physicians, hospital staff, and infection control personnel at receiving institutions must be adequately prepared to isolate and treat these patients (22,23). Previous studies of transmission from vancomycin-intermediate S. aureus (VISA)- or VRSA-colonized or infected patients show that these organisms can be transmitted to close contacts or other hospitalized patients (7,21,24).

Previous studies have also shown that carriage of VRE or MRSA may be persistent, which would increase the potential for co-colonized patients to transmit either or both of these organisms to other patients (25,26). A mathematical model
Note: The term model has a different meaning in model theory, a branch of mathematical logic. An artifact which is used to illustrate a mathematical idea is also called a mathematical model and this usage is the reverse of the sense explained below.
 of the transmission dynamics of VRE has suggested that persistent colonization is the most important factor for increasing the endemic prevalence of this organism in the hospital (26). Furthermore, the potential for prolonged co-colonization could increase the likelihood that these patients would experience sufficient selective pressure for emergence of VRSA.

Recent reviews by Reuf, Fridkin, and Cosgrove et al. have summarized risk factors associated with clinical culture positivity for VRSA and VISA (4,22,23). However, with only 3 reported cases of VRSA and [approximately equal to] 20 reported cases of VISA, the precision of statistical associations has been limited. Recent exposure to vancomycin and recent isolation of MRSA were identified as risk factors for VISA in addition to concurrent colonization or infection with VRE and MRSA. Among co-colonized patients in this study, [approximately equal to] 21% received vancomycin, 26% received piperacillin-tazobactam, and 17% received a fluoroquinolone fluoroquinolone /flu·o·ro·quin·o·lone/ (-kwin´o-lon) any of a subgroup of fluorine-substituted quinolones, having a broader spectrum of activity than nalidixic acid.

fluor·o·quin·o·lone
n.
 before culture results.

This study is the first to report the prevalence, risk factors, and clinical outcomes of patients with VRE/MRSA co-colonization upon admission to the ICU. We report several risk-factors for co-colonization, including that the odds of co-colonization for patients admitted to the MICU were >4 times greater than those of patients admitted to the SICU and that patients who received antimicrobial drugs within 1 year of admission had 3 times the odds of co-colonization as patients who had not received antimicrobial drugs during a previous admission.

Ray et al. assessed the prevalence of gastrointestinal S. aureus colonization among a convenience sample of 37 patients colonized with VRE and reported that 20 (54.1%) of these patients were also colonized with MRSA (27). However, comparing these results to those presented here is difficult, given the stark differences between patient groups. The study by Ray et al. included only hospitalized patients from whom a minimum of 3 stool samples (collected weekly) were obtained (i.e., inpatients with extended lengths of stay). We believe that ICU patients co-colonized with VRE and MRSA are at risk of acquiring and transmitting VRSA because they generally are exposed to greater antimicrobial selective pressure, have extended lengths of stay, greater likelihood of indwelling indwelling /in·dwell·ing/ (in´dwel-ing) pertaining to a catheter or other tube left within an organ or body passage for drainage, to maintain patency, or for the administration of drugs or nutrients.  devices, greater severity of illness, and are more likely to have a history of previous hospitalization and related exposures than patients admitted to general medical wards. Despite these differences, perirectal colonization of both organisms was similar between the patients in the study by Ray et al. and this study (54.1% vs. 40.3%, respectively). Other studies have also suggested a prevalence of VRE/MRSA co-colonization or co-infection ranging from 9.5% to 28.6%; however, these studies relied upon clinical cultures to provide these estimates (14,15).

A limitation of this study is that investigators were unable to determine the species of the VRE isolates. Historically, Enterococcus faecalis Enterococcus faecalis is a Gram-positive commensal bacterium inhabiting the gastrointestinal tracts of humans and other mammals.[1] Like other species in the genus Enterococcus, E.  has been more likely to be associated with conjugation conjugation, in genetics
conjugation, in genetics: see recombination.
conjugation, in grammar
conjugation: see inflection.
 events and subsequent VRSA colonization or infection compared with E. faecium (7,28). However, only 3 VRSA cases are known, and we are not aware of any biologic explanation for why E. faecium would be less likely to be involved in transmission of vancomycin resistance to MRSA compared with E. faecalis. Still, these data would have been useful and informative. A previous, hospitalwide study at UMMC suggested that among isolated VRE, the prevalence of E. faecium and E. faecalis were 87%, and 13%, respectively (29).

In summary, these data describe a high prevalence of patients co-colonized with VRE and MRSA on admission to an ICU at a tertiary-care hospital, none of whom would have been detected by clinical culture. Risk factors for VRE and MRSA co-colonization are also described. Given that many of these patients were discharged to other institutions, treating physicians and infection control personnel must be cognizant of the risks for VRSA colonization and infection and use appropriate precautions. Appropriate methods to rapidly detect co-colonized patients must be identified to suppress the emergence of VRSA; limit patient-to-patient transmission of MRSA, VRE, and VRSA; and prevent endemic VRSA colonization in healthcare institutions.

Acknowledgments

We thank Colleen Reilly and Jingkun Zhu for database maintenance and abstraction.

Financial support was provided by Veterans Affairs Veterans Affairs is a term of the business that deals with the relation between a government and its veteran communities, usually administered by the designated government agency.  Health Services Research Health services research is the multidisciplinary field of scientific investigation that studies how social factors, financing systems, organizational structures and processes, health technologies, and personal behaviors affect access to health care, the quality and cost of health care,  and Development Service Research Career Development Award (RCD-02026-1 to E.N.P.) and National Institutes of Health (K23 AI01752-01A1 to A.D.H.). Funding organizations provided salary support only for stated investigators.

References

(1.) National Nosocomial Infections Surveillance (NNIS NNIS National Nosocomial Infection Surveillance System ) System Report, data summary from January 1992 through June 2003, issued August 2003. Am J Infect Control. 2003;31:481-98.

(2.) Cosgrove SE, Sakoulas G, Perencevich EN, Schwaber M J, Karchmer

AW, Carmeli Y. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus Staphylococcus au·re·us
n.
A bacterium that causes furunculosis, pyemia, osteomyelitis, suppuration of wounds, and food poisoning.


Staphylococcus aureus Staphylococcus pyogenes
 bacteremia bacteremia: see septicemia.
bacteremia

Presence of bacteria in the blood. Short-term bacteremia follows dental or surgical procedures, especially if local infection or very high-risk surgery releases bacteria from isolated sites.
: a meta-analysis. Clin Infect Dis. 2003;36:53-9.

(3.) Murray BE. Vancomycin-resistant enterococcal infections. N Engl J Med. 2000;342:710-21.

(4.) Ruef C. Epidemiology and clinical impact of glycopeptide resistance in Staphylococcus aureus. Infection. 2004;32:315-27.

(5.) Whitener whit·en  
tr. & intr.v. whit·ened, whit·en·ing, whit·ens
To make or become white or whiter, especially by bleaching.



whit
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(6.) Tenover FC, Weigel LM, Appelbaum PC, McDougal LK, Chaitram J, McAllister S, et al. Vancomycin-resistant Staphylococcus aureus isolate from a patient in Pennsylvania. Antimicrob Agents Chemother. 2004;48:275-80.

(7.) Chang S, Sievert sie·vert
n.
Abbr. Sv A unit of ionizing radiation absorbed dose equivalent in the International System of Units, obtained as a product of the absorbed dose measure in grays and a dimensionless factor, stipulated by the International
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(8.) Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center. . Vancomycin-resistant Staphylococcus aureus Pennsylvania, 2002. MMWR MMWR Morbidity & Mortality Weekly Report Epidemiology A news bulletin published by the CDC, which provides epidemiologic data–eg, statistics on the incidence of AIDS, rabies, rubella, STDs and other communicable diseases, causes of mortality–eg,  Morb Mortal Wkly Rep. 2002;51:902.

(9.) Centers for Disease Control and Prevention. Vancomycin-resistant Staphylococcus aureus--New York, 2004. MMWR Morb Mortal Wkly Rep. 2004;53:322-3.

(10.) Centers for Disease Control and Prevention. Vancomycin-resistant Staphylococcus aureus--Pennsylvania, 2002. JAMA JAMA
abbr.
Journal of the American Medical Association
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(12.) Bonten MJ, Slaughter S, Ambergen AW, Hayden MK, van Voorbis J, Mathan C, et al. The role of "colonization pressure" in the spread of vancomycin-resistant enterococci: an important infection control variable. Arch Intern Med. 1998;158:1127-32.

(13.) McDonald JR, Engemann JJ, Kaye KS, Sexton DJ. Co-infection or co-colonization with vancomycin-resistant enterococci and methicillin-resistant Staphylococcus aureus in a network of community hospitals. Infect Control Hosp Epidemiol. 2004;25:622.

(14.) Franchi D, Climo MW, Wong AH, Edmond MB, Wenzel RP. Seeking vancomycin resistant Staphylococcus aureus among patients with vancomycin-resistant enterococci. Clin Infect Dis. 1999:29:1566-8.

(15.) Warren DK, Nitro A, Hill C, Fraser VJ, Kollef MH. Occurrence of co-colonization or co-infection with vancomycin-resistant enterococci and methicillin-resistant Staphylococcus aureus in a medical intensive care unit. Infect Control Hosp Epidemiol. 2004:25:99-104.

(16.) McGregor JC, Kim PW, Perencevich EN, Bradham DD, Furuno JP, Kaye KS, et al. Utility of the chronic disease score and Charlson comorbidity index as comorbidity measures for use in epidemiologic studies of antibiotic-resistant organisms. Am J Epidemiol. 2005;161:483-93.

(17.) Harris AD, Smith D, Johnson JA, Bradham DD, Roghmann MC. Risk factors for imipenem-resistant Pseudomonas aeruginosa Pseudomonas aeruginosa A normal soil inhabitant and human saprophyte that may contaminate various solutions in a hospital, causing opportunistic infection in weakened Pts Clinical Infective endocarditis in IVDAs, RTIs, UTIs, bacteremia, meningitis, 'malignant'  among hospitalized patients. Clin Infect Dis. 2002;34:340-5.

(18.) Furuno JR Harris AD. Wright MO, McGregor JC, Venezia RA, Zhu J, et al. Prediction rules to identify patients with methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci upon hospital admission. Am J Infect Control. 2004;32:436-40.

(19.) Kim PW, Harris AD, Roghmann MC, Morris JG Jr. Strinivasan A, Perencevich EN. Epidemiological risk factors for isolation of ceftriaxone-resistant versus -susceptible Citrobacter freundii Citrobacter freundii Microbiology A Citrobacter opportunistic pathogen Management Cephalothin, aminoglycosides  in hospitalized patients. Antimicrob Agents Chemother. 2003;47:2882-7.

(20.) Deyo RA, Cherkin DC, Ciol MA. Adapting a clinical comorbidity index for use with ICD-9-CM ICD-9-CM International Classification of Disease, 9th edition, Clinical Modification
A standardized classification of disease, injuries, and causes of death, by etiology and anatomic localization and codified into a 6-digit number, which allows
 administrative databases. J Clin Epidemiol. 1992;45:613-9.

(21.) Smith TL, Pearson ML, Wilcox KR, Cruz C, Lancaster MV, Robinson-Dunn B, et ah Emergence of vancomycin resistance in Staphylococcus aureus. Glycopeptide-intermediate Staphylococcus aureus Working Group. N Engl J Med. 1999;340:493-501.

(22.) Fridkin SK. Vancomycin-intermediate and -resistant Staphylococcus aureus: what the infections disease specialist needs to know. Clin Infect Dis. 2001;32:108-15.

(23.) Cosgrove SE, Carroll KC, Perl TM. Staphylococcus aureus with reduced susceptibility to vancomycin. Clin Infect Dis. 2004;39:5394-5.

(24). Srinivasan A, Dick JD, Perl TM. Vancomycin resistance in staphylococci staph·y·lo·coc·cus  
n. pl. staph·y·lo·coc·ci
A spherical gram-positive parasitic bacterium of the genus Staphylococcus, usually occurring in grapelike clusters and causing boils, septicemia, and other infections.
. Clin Microbiol Rev. 2002;15:430-8.

(25.) Harbarth S, Liassine N, Dharan S, Herrault P, Auckenthaler R, Pittet D. Risk factors for persistent carriage of methicillin-resistant Staphylococcus aureus. Clin Infect Dis. 2000;31:1380-5.

(26). D'Agata EM, Horn MA, Webb GF. The impact of persistent gastrointestinal colonization on the transmission dynamics of vancomycin-resistant enterococci. J Infect Dis. 2002;185:766-73.

(27.) Ray AJ, Pultz NJ, Bhalla A, Aron DC, Donskey CJ. Coexistence of vancomycin-resistant enterococci and Staphylococcus altreus in the intestinal tracts of hospitalized patients. Clin Infect Dis. 2003;37:875-81.

(28.) Noble WC, Virani Z, Cree RG. Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC NCTC National Conservation Training Center
NCTC National Counterterrorism Center (9/11 Commission Report)
NCTC National Cable Television Cooperative
NCTC National Collection of Type Cultures (UK laboratory) 
 12201 to Staphylococcus aureus. FEMS FEMS Federation of European Microbiological Societies
FEMS Federation of European Materials Societies
FEMS Fabrication Engineering Management System
FEMS Facility Equipment Maintenance System (PMEL/TMDE) 
 Microbiol Lett. 1992;72:195-8.

(29.) Morris JG Jr, Shay shay  
n. Informal
A chaise.



[Back-formation from chaise (taken as pl. )]

Noun 1.
 DK, Hebden JN, McCarter RJ Jr, Perdue Perdue may refer to:
  • Perdue, Saskatchewan, Canada
  • Perdue Farms, an American chicken-farming corporation
  • Perdue School of Business, in Salisbury University, Salisbury, Maryland
People with the surname Perdue
 BE, Jarvis W, et al. Enterococci resistant to multiple antimicrobial agents Antimicrobial agents

Chemical compounds biosynthetically or synthetically produced which either destroy or usefully suppress the growth or metabolism of a variety of microscopic or submicroscopic forms of life.
, including vancomycin. Establishment of endemicity in a university medical center. Ann Intern Med. 1995;123:250-9.

Jon P. Furuno, * Eli N. Perencevich, * ([dagger]) ([double dagger]) Judith A. Johnson, * ([dagger]) Marc-Oliver Wright, ([double dagger]) (2) Jessina C. McGregor, * J. Glenn Morris Jr, * ([dagger]) Sandra M. Strauss, * Mary-Claire Roghman, * ([dagger]) Lucia L. Nemoy, * ([dagger]) Harold C. Standiford, ([double dagger]) Joan N. Hebden, ([double dagger]) and Anthony D. Harris * ([dagger]) ([double dagger])

* University of Maryland School of Medicine, Baltimore, Maryland, USA; ([dagger]) Veteran's Affairs Maryland Health Care System, Baltimore, Maryland, USA; and ([double dagger]) University of Maryland Medical Center, Baltimore, Maryland, USA

(1) These data were presented in part at the 44th Interscience Conference on Antimicrobial Agents and Chemotherapy Antimicrobial Agents and Chemotherapy (print-ISSN 0066-4804, CODEN AMACCQ; canceled ISSN 0074-9923, canceled CODEN AACHAX) is an academic journal published by the American Society for Microbiology. , Washington DC, September 2004.

(2) Current affiliation: Marshfield Clinic Research Foundation, Marshfield, Wisconsin, USA.

Dr Furuno is an instructor in the Department of Epidemiology and Preventive Medicine preventive medicine, branch of medicine dealing with the prevention of disease and the maintenance of good health practices. Until recently preventive medicine was largely the domain of the U.S.  at the University of Maryland School of Medicine and coordinator of the Maryland Foodborne Diseases Active Surveillance Network (FoodNet). His primary research interests include antimicrobial resistance, foodborne disease, and epidemiologic methodology.

Address for correspondence: Jon P. Euruno, Department of Epidemiology and Preventive Medicine, University of Maryland School of Medicine, 100 N Greene St, Lower Level, Baltimore, MD 21201, USA: Fax: 410-706-0098; email: jfuruno@epi.umaryland.edu
Table 1. Characteristics of the study population by co-colonization
status *

                                      MRSA/VRE          No
                                        co-            co-
                                    colonization   colonization     p
Characteristic                        (n = 65)     (n = 2,375)    value

Demographic variable
  Mean age, y (SD)                  61.1 (15.1)    55.7 (16.0)    <0.01
  Male sex, n (%)                    43 (66.2)     1,277 (53.8)    0.05
Variables from current admission
  Type of ICU (MICU), n (%)          49 (75.4)     1,014 (42.7)   <0.01
  Transfer from another hospital,    10 (15.4)      711 (29.9)    <0.01
    n (%)
  Comorbidities
    HIV/AIDS, n (%)                   3 (4.6)        77 (3.2)      0.54
    Malignancy, n (%)                 6 (9.2)       423 (17.8)     0.07
    Cardiac disease, n (%)           20 (30.8)      486 (20.5)     0.04
    Diabetes mellitus, n (%)         14 (21.5)      486 (20.5)     0.83
    Liver disease, n (%)              2 (3.1)       182 (7.7)      0.17
    Renal disease, n (%)              3 (4.6)        74 (3.1)      0.50
Mean Charlson comorbidity score      2.1 (2.2)      2.3 (2.3)      0.37
  (SD)
Antimicrobial drugs before
    culture
  Vancomycin, n (%)                  14 (21.5)      226 (9.5)     <0.01
  Piperacillin-tazobactam, n (%)     17 (26.2)      398 (16.8)     0.05
  Imipenem, n (%)                     2 (3.1)        72 (3.0)      0.98
  Cephalosporins, n (%)               7 (10.8)      426 (17.9)     0.14
  Aminoglycosides, n (%)              4 (6.2)       109 (4.6)      0.55
  Fluoroquinolones, n (%)            11 (16.9)      223 (9.4)      0.04
Variables from previous
    admissions
  Previous MRSA colonization/        31 (47.7)      145 (6.1)     <0.01
    infection
  Previous VRE colonization/         18 (27.7)      178 (7.5)     <0.01
    infection
  Hospital admission (<1 y),         37 (57.9)      751 (31.6)    <0.01
    n (%)
  ICU admission (<1 y), n (%)        17 (26.2)      309 (13.0)    <0.01
  Antimicrobial drugs during         33 (50.8)      606 (25.5)    <0.01
    admission (<1 y), n (%)

* MRSA, methicillin-resistant Staphylococcus aureus; VRE,
vancomycin-resistant enterococci; SD, standard deviation, ICU,
intensive care unit, MICU, medical ICU.

Table 2. Components of final logistic regression models *

                                 MRSA/VRE             VRE
                             co-colonization,    colonization,
Characteristic                 OR (95% CI)        OR (95% CI)

Age                          1.03 (1.01-1.05)
Male sex                     1.93 (1.14-3.3)
Admission to MICU            4.38 (2.46-7.81)   1.84 (1.38-2.46)
Antimicrobial drugs during   3.06 (1.85-5.07)   3.38 (2.54-4.51)
  prior admission (<1 y)
Diabetes mellitus                               1.39 (1.00-1.83)
Liver disease                                   1.64 (1.04-2.58)
Renal disease                                   2.28 (1.26-4.1)
Vancomycin                                      1.54 (1.03-2.31)
Piperacillin-tazobactam                         1.77 (1.27-2.47)
Imipenem                                        2.47 (1.40-4.36)
Fluoroquinolones                                2.01 (1.37-2.96)
HIV/AIDS

                                  MRSA
                              colonization,
Characteristic                 OR (95% CI)

Age
Male sex
Admission to MICU
Antimicrobial drugs during   1.66 (1.20-2.30)
  prior admission (<1 y)
Diabetes mellitus            1.83 (1.30-2.58)
Liver disease
Renal disease
Vancomycin
Piperacillin-tazobactam
Imipenem
Fluoroquinolones
HIV/AIDS                     2.74 (1.46-5.14)

* Only variables significantly associated with the outcome are
included in the final models. MRSA, methicillin-resistant
Staphylococcus aureus; VRE, vancomycin-resistant enterococci;
OR, odds ratio; CI, confidence interval; MICU, medical
intensive care unit.

Table 3. Outcomes of patients co-colonized with VRE and MRSA *

                                MRSA/VRE
                                   co-           No co-
                              colonization,   colonization,
Outcome                          n = 65         n = 2,375     p value

Death, n (%)                    16 (24.6)      420 (17.7)       0.15
Mean length (d) of hospital    12.0 (16.5)     14.0 (17.8)      0.37
  stay (SD)
Subsequent MRSA-positive         2 (3.1)        34 (1.4)       <0.01
  clinical culture, n (%)
Subsequent VRE-positive          2 (3.1)        39 (1.6)        0.38
  clinical culture, n (%)
Discharge location
  Home or self-care, n (%)      27 (41.5)     1,467 (61.8)     <0.01
  Hospital, n (%)               21 (32.3)      368 (15.5)      <0.01
  Rehabilitation facility,       1 (1.5)        62 (2.6)        0.59
    n (%)
  Unknown, n (%)                    0           18 (0.8)        0.48

* VRE, vancomycin-resistant enterococci; MRSA, methicillin-resistant
Staphylococcus aureus; SD, standard deviation.
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Author:Harris, Anthony D.
Publication:Emerging Infectious Diseases
Geographic Code:1USA
Date:Oct 1, 2005
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