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ARTICLE |

Strategies to Prevent and Control the Emergence and Spread of Antimicrobial-Resistant Microorganisms in Hospitals: Title and subTitle BreakA Challenge to Hospital Leadership FREE

Donald A. Goldmann, MD; Robert A. Weinstein, MD; Richard P. Wenzel, MD; Ofelia C. Tablan, MD; Richard J. Duma, MD; Robert P. Gaynes, MD; James Schlosser, MD; William J. Martone, MD; Jacques Acar, MD; Jerry Avorn, MD; John Burke, MD; John Boyce, MD; Jean Carlet, MD; Julia Garner, RN, MN, CDC; Mary J. Gilchrist, PhD; Elaine Larson, RN, PhD; James Lee, MD, PhD; Mark A. Malangoni, MD; Edward McSweegan, PhD; John McGowan, MD; Armando D. Meza, MD; Joel Moses, MD; Carole Patterson, RN, MN; Bruce C. Perry, MD, MPH; Barbara Russell, RN, MPH; Jerome Schentag, PharmD; Albert T. Sheldon, Jr, PhD; Jane Siegel, MD; Ken Spitalny, MD; James Tenney, MD; Fred Tenover, PhD, CDC; Ralph Timperi, PhD; Jan Maarten van den Berg, MD
[+] Author Affiliations

A complete list of the workshop participants appears at the end of this article.

The workshop, Antimicrobial Resistance in Hospitals; Strategies to Improve Antimicrobial Use and Prevent Nosocomial Transmission of Antimicrobial-Resistant Microorganisms, was held on September 12-14, 1994, in Atlanta, Ga, under the joint sponsorship of the Centers for Disease Control and Prevention and the National Foundation for Infectious Diseases.

Reprint requests to Division of Infectious Diseases, Children's Hospital, 300 Longwood Ave, Boston, MA 02115 (Dr Goldmann).


JAMA. 1996;275(3):234-240. doi:10.1001/jama.1996.03530270074035
Text Size: A A A
Published online

Objective.  —To provide hospital leaders with strategic goals or actions likely to have a significant impact on antimicrobial resistance, outline outcome and process measures for evaluating progress toward each goal, describe potential barriers to success, and suggest countermeasures and novel improvement strategies.

Participants.  —A multidisciplinary group of experts was drawn from the following areas: hospital epidemiology and infection control, infectious diseases (including graduate training programs), clinical practice (including nursing, surgery, internal medicine, and pediatrics), pharmacy, administration, quality improvement, appropriateness evaluation, behavior modification, practice guideline development, medical informatics, and outcomes research. Representatives from appropriate federal agencies, the Joint Commission on Accreditation of Healthcare Organizations, and the pharmaceutical industry also participated.

Evidence.  —Published literature, guidelines, expert opinion, and practical experience regarding efforts to improve antibiotic utilization and prevent and control the emergence and dissemination of antimicrobial-resistant microorganisms in hospitals.

Consensus Process.  —Participants were divided into two quality improvement teams: one focusing on improving antimicrobial usage and the other on preventing and controlling transmission of resistant microorganisms. The teams modeled the process a hospital might use to develop and implement a strategic plan to combat antimicrobial resistance.

Conclusions.  —Ten strategic goals and related process and outcome measures were agreed on. The five strategic goals to optimize antimicrobial use were as follows: optimizing antimicrobial prophylaxis for operative procedures; optimizing choice and duration of empiric therapy; improving antimicrobial prescribing by educational and administrative means; monitoring and providing feedback regarding antibiotic resistance; and defining and implementing health care delivery system guidelines for important types of antimicrobial use. The five strategic goals to detect, report, and prevent transmission of antimicrobial resistant organisms were as follows: to develop a system to recognize and report trends in antimicrobial resistance within the institution; develop a system to rapidly detect and report resistant microorganisms in individual patients and ensure a rapid response by caregivers; increase adherence to basic infection control policies and procedures; incorporate the detection, prevention, and control of antimicrobial resistance into institutional strategic goals and provide the required resources; and develop a plan for identifying, transferring, discharging, and readmitting patients colonized with specific antimicrobial-resistant pathogens.(JAMA. 1996;275:234-240)

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Ranson MR, Oppenheim BA, Jackson A, Kamthan AG, Scarffe JH.  Double-blind placebo controlled study of vancomycin prophylaxis for central venous catheter insertion in cancer patients. J Hosp Infect . 1990;; 15:95-102.
Gaillard JL, Merlino R, Pajot N, et al.  Conventional and nonconventional modes of vancomycin administration to decontaminate the internal surface of catheters colonized with coagulase-negative staphylococci. J Parenter Enteral Nutr . 1990;;14:593-597.
Spafford PS, Sinkin RA, Cox C, Reubens L, Powell KR.  Prevention of central venous catheter-related coagulase-negative staphylococcal sepsis in neonates. J Pediatr . 1994;;125:259-263.
Centers for Disease Control and Prevention.  Nosocomial enterococci resistant to vancomycin: United States, 1989-1993. MMWR Morb Mortal Wkly Rep . 1993;;42:597-599.
Murray BE.  The life and times of the enterococcus. Clin Microbiol Rev . 1990;;3:46-65.
Schaberg DR, Dillon WI, Robinson KA, Bradley SF.  Increasing resistance of enterococci to ciprofloxacin. Antimicrob Agents Chemother . 1992;;36:2533-2535.
Zervos MJ, Kauffman CA, Therasse PM, Bergman AG, Mikesell TS, Schaberg DR.  Nosocomial infection by gentamicin-resistant Streptococcus faecalis. Ann Intern Med . 1987;;106:687-691.
Huycke MM, Spiegel CA, Gilmore MS.  Bacteremia caused by hemolytic, high-level gentamicin-resistant Enterococcus faecalis. Antimicrob Agents Chemother . 1991;;35:1626-1634.
Rydberg J, Larsson C, Miorner H.  Resistance to fluoroquinolones in Pseudomonas aeruginosa and Klebsiella pneumoniae. Scand J Infect Dis . 1994;;26: 317-320.
Rice LB, Willey SH, Papanicolaou GA, et al.  Outbreak of ceftazidime resistance caused by extended-spectrum beta-lactamases at a Massachusetts chronic-care facility. Antimicrob Agents Chemother . 1990;; 34:2193-2199.
Jarlier V, Nicolas MH, Fournier G, Philippon A.  Extended broad-spectrum beta-lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae. Rev Infect Dis . 1988;; 10:867-878.
Osano E, Arakawa Y, Wacharotayankun R, et al.  Molecular characterization of an enterobacterial metallo beta-lactamase found in a clinical isolate of Serratia marcescens that shows imipenem resistance. Antimicrob Agents Chemother . 1994;;38:71-78.
Watanabe N, Hiruma R, Katsu K.  Comparative in-vitro activities of newer cephalosporins cefclidin, cefepime, and cefpirome against ceftazidime- or imipenem-resistant Pseudomonas aeruginosa. J Antimicrob Chemother . 1992;;30:633-641.
Wingard JR.  Infections due to resistant Candida species in patients with cancer who are receiving chemotherapy. Clin Infect Dis . 1994;;19( (suppl 1) ):S49-S53.
Ruhnke M, Eigler A, Tennagen I, Geiseler B, Engelman E, Trautmann M.  Emergence of fluconazole-resistant strains of Candida albicans in patients with recurrent oropharyngeal candidosis and human immunodeficiency virus infection. J Clin Microbiol . 1994;;32:2092-2098.
Dance DA, Pearson AD, Seal DV, Lowes JA.  A hospital outbreak caused by a chlorhexidine and antibiotic-resistant Proteus mirabilis. J Hosp Infect . 1987;;10:10-16.
Baillie L.  Chlorhexidine resistance among bacteria isolated from urine of catheterized patients. J Hosp Infect . 1987;;10:83-86.
Udo EE, Pearman JW, Grubb WB.  Emergence of high-level mupirocin resistance in methicillin-resistant Staphylococcus aureus in Western Australia. J Hosp Infect . 1994;;26:157-165.
Connolly S, Noble WC, Phillips I.  Mupirocin resistance in coagulase-negative staphylococci. J Med Microbiol . 1993;;39:450-453.
Naguib MH, Naguib MT.  Mupirocin resistance in methicillin-resistant Staphylococcus aureus from a veterans hospital. Chemotherapy . 1993;;39:400-404.
Billstein SA.  How the pharmaceutical industry brings an antibiotic drug to market in the United States. Antimicrob Agents Chemother . 1994;;38:2679-2682.
Cohen ML.  Epidemiology of drug resistance. Science . 1992;;257:1050-1055.
Kunin CM, Lipton HL, Tupasi T, et al.  Social, behavioral, and practical factors affecting antibiotic use worldwide: report of Task Force 4. Rev Infect Dis . 1987;;9( (suppl 3) ):S270-S285.
Riley LW, Ceballos BS, Trabulsi LR, Toledo MRF, Blake PA.  The significance of hospitals as reservoirs for endemic multi-resistant Salmonella typhimurium causing infection in urban Brazilian children. J Infect Dis . 1984;;150:236-241.
Reichler M, Rakovsky J, Sobotova A, et al.  Multiple antimicrobial resistance of pneumococci in children with otitis media, bacteremia, and meningitis in Slovakia. J Infect Dis . 1995;;171:1491-1496.
Dellinger EP, Gross PA, Barrett TL, et al.  Quality standard for antimicrobial prophylaxis in surgical procedures. Clin Infect Dis . 1994;;18:422-427.
Larson E.  Guidelines for use of topical antimicrobial agents. Am J Infect Control . 1988;;16:253-266.
Gross PA, Barrett TL, Dellinger EP, et al.  Quality standard for the treatment of bacteremia: Infectious Diseases Society of America. Clin Infect Dis . 1994;;18:428-430.
Evans RS, Pestotnik SL, Burke JP, Gardner RM, Larsen RA, Classen DC.  Reducing the duration of prophylactic antibiotic use through computer monitoring of surgical patients. DICP . 1990;;24:351-354.
Woodward RS, Medoff G, Smith MD, Gray JL.  Antibiotic cost savings from formulary restrictions and physician monitoring in a medical-school—affiliated hospital. Am J Med . 1987;;83:817-823.
Albert RK, Condie F.  Hand-washing patterns in medical intensive care units. N Engl J Med . 1981;; 304:146-147.
Sproat LJ, Inglis TJ.  A multicentre survey of hand hygiene practice in intensive care units. J Hosp Infect . 1994;;26:137-148.
Lohr JA, Ingram DL, Dudley SM, Lawton EL, Donowitz LG.  Hand washing in pediatric ambulatory settings. AJDC . 1991;;145:1198-1199.
Doebbeling BN, Stanley GL, Sheetz CT, et al.  Comparative efficacy of alternative hand-washing agents in reducing nosocomial infections in intensive care units. N Engl J Med . 1992;;327:88-93.
Jarvis WR.  Handwashing: the Semmelweis lesson forgotten? Lancet . 1994;;344:1312-1313.
Goldmann DA.  Hand-washing and nosocomial infections. N Engl J Med . 1992;;327:120-122.
Dubbert PM, Dolce J, Richter W, Miller M, Chapman SW.  Increasing intensive care unit staff hand-washing: effects of education and group feedback. Infect Control Hosp Epidemiol . 1990;;11:191-193.
Conly JM, Hill S, Ross J, Leitzman J, Louie TJ.  Handwashing practices in an intensive care unit: the effects of an educational program and its relationship to infection rates. Am J Infect Control . 1989;; 17:330-339.
Larson E, McGreer A, Quraishi ZA, et al.  Effect of an automated sink on handwashing practices and attitudes in high-risk units. Infect Control Hosp Epidemiol . 1991;;12:422-428.
Maki DG, McCormick RD, Zilz MA, et al. An MRSA outbreak in a surgical intensive care unit during universal precautions: new epidemiology for nosocomial MRSA; downside of universal precautions (UPs). In: Abstracts of the 30th Interscience Conference on Antimicrobial Agents and Chemotherapy; October 21-24, 1990; Atlanta, Ga.
Centers for Disease Control.  Update: universal precautions for prevention of transmission of human immunodeficiency virus, hepatitis B virus, and blood-borne pathogens in health-care settings. MMWR Morb Mortal Wkly Rep . 1988;;37:377-388.
Lynch P, Jackson MM, Cummings MJ, Stamm WE.  Rethinking the role of isolation practices in the prevention of nosocomial infections. Ann Intern Med . 1987;;107:243-246.
Garner JS, the Hospital Infection Control Practices Advisory Committee.  Guidelines for isolation precautions in hospitals. Hosp Epidemiol . In press.
Haley RW, Bregman DA.  The role of understaffing and overcrowding in recurrent outbreaks of staphylococcal infection in a neonatal special-care unit. J Infect Dis . 1982;;145:875-885.
Goldmann DA, Durbin WA Jr, Freeman J.  Nosocomial infections in a neonatal intensive care unit. J Infect Dis . 1981;;144:449-459.
Weinstein RA.  Epidemiology and control of nosocomial infections in adult intensive care units. Am J Med . 1991;;30:2525-2528.
Hartstein AI, Rashad AL, Liebler JM, et al.  Multiple intensive care unit outbreaks of Acinetobacter calcoaceticus subspecies anitratus respiratory infection and colonization associated with contaminated, reusable ventilator circuits and resuscitation bags. Am J Med . 1988;;85:624-631.
Flynn DM, Weinstein RA, Kabins SA.  Infections with gram-negative bacilli in a cardiac surgery intensive care unit: the relative role of Enterobacter. J Hosp Infect . 1988;;11( (suppl A) ):367-373.
Johanson WG, Pierce AK, Sanford JP.  Changing bacterial flora of hospitalized patients. N Engl J Med . 1969;;281:1137-1140.
Johanson WG Jr, Pierce AK, Sanford JP, Thomas GD.  Nosocomial respiratory infections with gram-negative bacilli. Ann Intern Med . 1972;;77:701-706.
Goldmann DA, Leclair J, Macone A.  Bacterial colonization of neonates admitted to an intensive care environment. J Pediatr . 1978;;93:288-293.
Allen KD, Bartzokas CA, Graham R, Gibson MF, Gilbertson AA.  Acquisition of endemic Pseudomonas aeruginosa on an intensive therapy unit. J Hosp Infect . 1987;;10:156-164.
Gorman LJ, Sanai L, Notman AW, Grant IS, Masterton RG.  Cross-infection in an intensive care unit by Klebsiella pneumoniae from ventilator condensate. J Hosp Infect . 1993;;23:27-34.
Wade JJ, Desai N, Casewell MW.  Hygienic hand disinfection for the removal of epidemic vancomycin-resistant Enterococcus faecium and gentamicin-resistant Enterobacter cloacae. J Hosp Infect . 1991;;18: 211-218.
Ehrenkranz NJ, Alfonso BC.  Failure of bland soap handwash to prevent hand transfer of patient bacteria to urethral catheters. Infect Control Hosp Epidemiol . 1991;;12:654-662.
Maki DG, Alvarado CJ, Hassemer MA, Zilz MA.  Relation of the inanimate hospital environment to endemic nosocomial infections. N Engl J Med . 1982;; 307:1562-1566.
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Country-Specific Mortality and Growth Failure in Infancy and Yound Children and Association With Material Stature

Use interactive graphics and maps to view and sort country-specific infant and early dhildhood mortality and growth failure data and their association with maternal

Panlilio AL, Culver DH, Gaynes RP, et al.  Methicillin-resistant Staphylococcus aureus in U.S. hospitals, 1975-1991. Infect Control Hosp Epidemiol . 1992;;13:582-586.
Ranson MR, Oppenheim BA, Jackson A, Kamthan AG, Scarffe JH.  Double-blind placebo controlled study of vancomycin prophylaxis for central venous catheter insertion in cancer patients. J Hosp Infect . 1990;; 15:95-102.
Gaillard JL, Merlino R, Pajot N, et al.  Conventional and nonconventional modes of vancomycin administration to decontaminate the internal surface of catheters colonized with coagulase-negative staphylococci. J Parenter Enteral Nutr . 1990;;14:593-597.
Spafford PS, Sinkin RA, Cox C, Reubens L, Powell KR.  Prevention of central venous catheter-related coagulase-negative staphylococcal sepsis in neonates. J Pediatr . 1994;;125:259-263.
Centers for Disease Control and Prevention.  Nosocomial enterococci resistant to vancomycin: United States, 1989-1993. MMWR Morb Mortal Wkly Rep . 1993;;42:597-599.
Murray BE.  The life and times of the enterococcus. Clin Microbiol Rev . 1990;;3:46-65.
Schaberg DR, Dillon WI, Robinson KA, Bradley SF.  Increasing resistance of enterococci to ciprofloxacin. Antimicrob Agents Chemother . 1992;;36:2533-2535.
Zervos MJ, Kauffman CA, Therasse PM, Bergman AG, Mikesell TS, Schaberg DR.  Nosocomial infection by gentamicin-resistant Streptococcus faecalis. Ann Intern Med . 1987;;106:687-691.
Huycke MM, Spiegel CA, Gilmore MS.  Bacteremia caused by hemolytic, high-level gentamicin-resistant Enterococcus faecalis. Antimicrob Agents Chemother . 1991;;35:1626-1634.
Rydberg J, Larsson C, Miorner H.  Resistance to fluoroquinolones in Pseudomonas aeruginosa and Klebsiella pneumoniae. Scand J Infect Dis . 1994;;26: 317-320.
Rice LB, Willey SH, Papanicolaou GA, et al.  Outbreak of ceftazidime resistance caused by extended-spectrum beta-lactamases at a Massachusetts chronic-care facility. Antimicrob Agents Chemother . 1990;; 34:2193-2199.
Jarlier V, Nicolas MH, Fournier G, Philippon A.  Extended broad-spectrum beta-lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae. Rev Infect Dis . 1988;; 10:867-878.
Osano E, Arakawa Y, Wacharotayankun R, et al.  Molecular characterization of an enterobacterial metallo beta-lactamase found in a clinical isolate of Serratia marcescens that shows imipenem resistance. Antimicrob Agents Chemother . 1994;;38:71-78.
Watanabe N, Hiruma R, Katsu K.  Comparative in-vitro activities of newer cephalosporins cefclidin, cefepime, and cefpirome against ceftazidime- or imipenem-resistant Pseudomonas aeruginosa. J Antimicrob Chemother . 1992;;30:633-641.
Wingard JR.  Infections due to resistant Candida species in patients with cancer who are receiving chemotherapy. Clin Infect Dis . 1994;;19( (suppl 1) ):S49-S53.
Ruhnke M, Eigler A, Tennagen I, Geiseler B, Engelman E, Trautmann M.  Emergence of fluconazole-resistant strains of Candida albicans in patients with recurrent oropharyngeal candidosis and human immunodeficiency virus infection. J Clin Microbiol . 1994;;32:2092-2098.
Dance DA, Pearson AD, Seal DV, Lowes JA.  A hospital outbreak caused by a chlorhexidine and antibiotic-resistant Proteus mirabilis. J Hosp Infect . 1987;;10:10-16.
Baillie L.  Chlorhexidine resistance among bacteria isolated from urine of catheterized patients. J Hosp Infect . 1987;;10:83-86.
Udo EE, Pearman JW, Grubb WB.  Emergence of high-level mupirocin resistance in methicillin-resistant Staphylococcus aureus in Western Australia. J Hosp Infect . 1994;;26:157-165.
Connolly S, Noble WC, Phillips I.  Mupirocin resistance in coagulase-negative staphylococci. J Med Microbiol . 1993;;39:450-453.
Naguib MH, Naguib MT.  Mupirocin resistance in methicillin-resistant Staphylococcus aureus from a veterans hospital. Chemotherapy . 1993;;39:400-404.
Billstein SA.  How the pharmaceutical industry brings an antibiotic drug to market in the United States. Antimicrob Agents Chemother . 1994;;38:2679-2682.
Cohen ML.  Epidemiology of drug resistance. Science . 1992;;257:1050-1055.
Kunin CM, Lipton HL, Tupasi T, et al.  Social, behavioral, and practical factors affecting antibiotic use worldwide: report of Task Force 4. Rev Infect Dis . 1987;;9( (suppl 3) ):S270-S285.
Riley LW, Ceballos BS, Trabulsi LR, Toledo MRF, Blake PA.  The significance of hospitals as reservoirs for endemic multi-resistant Salmonella typhimurium causing infection in urban Brazilian children. J Infect Dis . 1984;;150:236-241.
Reichler M, Rakovsky J, Sobotova A, et al.  Multiple antimicrobial resistance of pneumococci in children with otitis media, bacteremia, and meningitis in Slovakia. J Infect Dis . 1995;;171:1491-1496.
Dellinger EP, Gross PA, Barrett TL, et al.  Quality standard for antimicrobial prophylaxis in surgical procedures. Clin Infect Dis . 1994;;18:422-427.
Larson E.  Guidelines for use of topical antimicrobial agents. Am J Infect Control . 1988;;16:253-266.
Gross PA, Barrett TL, Dellinger EP, et al.  Quality standard for the treatment of bacteremia: Infectious Diseases Society of America. Clin Infect Dis . 1994;;18:428-430.
Evans RS, Pestotnik SL, Burke JP, Gardner RM, Larsen RA, Classen DC.  Reducing the duration of prophylactic antibiotic use through computer monitoring of surgical patients. DICP . 1990;;24:351-354.
Woodward RS, Medoff G, Smith MD, Gray JL.  Antibiotic cost savings from formulary restrictions and physician monitoring in a medical-school—affiliated hospital. Am J Med . 1987;;83:817-823.
Albert RK, Condie F.  Hand-washing patterns in medical intensive care units. N Engl J Med . 1981;; 304:146-147.
Sproat LJ, Inglis TJ.  A multicentre survey of hand hygiene practice in intensive care units. J Hosp Infect . 1994;;26:137-148.
Lohr JA, Ingram DL, Dudley SM, Lawton EL, Donowitz LG.  Hand washing in pediatric ambulatory settings. AJDC . 1991;;145:1198-1199.
Doebbeling BN, Stanley GL, Sheetz CT, et al.  Comparative efficacy of alternative hand-washing agents in reducing nosocomial infections in intensive care units. N Engl J Med . 1992;;327:88-93.
Jarvis WR.  Handwashing: the Semmelweis lesson forgotten? Lancet . 1994;;344:1312-1313.
Goldmann DA.  Hand-washing and nosocomial infections. N Engl J Med . 1992;;327:120-122.
Dubbert PM, Dolce J, Richter W, Miller M, Chapman SW.  Increasing intensive care unit staff hand-washing: effects of education and group feedback. Infect Control Hosp Epidemiol . 1990;;11:191-193.
Conly JM, Hill S, Ross J, Leitzman J, Louie TJ.  Handwashing practices in an intensive care unit: the effects of an educational program and its relationship to infection rates. Am J Infect Control . 1989;; 17:330-339.
Larson E, McGreer A, Quraishi ZA, et al.  Effect of an automated sink on handwashing practices and attitudes in high-risk units. Infect Control Hosp Epidemiol . 1991;;12:422-428.
Maki DG, McCormick RD, Zilz MA, et al. An MRSA outbreak in a surgical intensive care unit during universal precautions: new epidemiology for nosocomial MRSA; downside of universal precautions (UPs). In: Abstracts of the 30th Interscience Conference on Antimicrobial Agents and Chemotherapy; October 21-24, 1990; Atlanta, Ga.
Centers for Disease Control.  Update: universal precautions for prevention of transmission of human immunodeficiency virus, hepatitis B virus, and blood-borne pathogens in health-care settings. MMWR Morb Mortal Wkly Rep . 1988;;37:377-388.
Lynch P, Jackson MM, Cummings MJ, Stamm WE.  Rethinking the role of isolation practices in the prevention of nosocomial infections. Ann Intern Med . 1987;;107:243-246.
Garner JS, the Hospital Infection Control Practices Advisory Committee.  Guidelines for isolation precautions in hospitals. Hosp Epidemiol . In press.
Haley RW, Bregman DA.  The role of understaffing and overcrowding in recurrent outbreaks of staphylococcal infection in a neonatal special-care unit. J Infect Dis . 1982;;145:875-885.
Goldmann DA, Durbin WA Jr, Freeman J.  Nosocomial infections in a neonatal intensive care unit. J Infect Dis . 1981;;144:449-459.
Weinstein RA.  Epidemiology and control of nosocomial infections in adult intensive care units. Am J Med . 1991;;30:2525-2528.
Hartstein AI, Rashad AL, Liebler JM, et al.  Multiple intensive care unit outbreaks of Acinetobacter calcoaceticus subspecies anitratus respiratory infection and colonization associated with contaminated, reusable ventilator circuits and resuscitation bags. Am J Med . 1988;;85:624-631.
Flynn DM, Weinstein RA, Kabins SA.  Infections with gram-negative bacilli in a cardiac surgery intensive care unit: the relative role of Enterobacter. J Hosp Infect . 1988;;11( (suppl A) ):367-373.
Johanson WG, Pierce AK, Sanford JP.  Changing bacterial flora of hospitalized patients. N Engl J Med . 1969;;281:1137-1140.
Johanson WG Jr, Pierce AK, Sanford JP, Thomas GD.  Nosocomial respiratory infections with gram-negative bacilli. Ann Intern Med . 1972;;77:701-706.
Goldmann DA, Leclair J, Macone A.  Bacterial colonization of neonates admitted to an intensive care environment. J Pediatr . 1978;;93:288-293.
Allen KD, Bartzokas CA, Graham R, Gibson MF, Gilbertson AA.  Acquisition of endemic Pseudomonas aeruginosa on an intensive therapy unit. J Hosp Infect . 1987;;10:156-164.
Gorman LJ, Sanai L, Notman AW, Grant IS, Masterton RG.  Cross-infection in an intensive care unit by Klebsiella pneumoniae from ventilator condensate. J Hosp Infect . 1993;;23:27-34.
Wade JJ, Desai N, Casewell MW.  Hygienic hand disinfection for the removal of epidemic vancomycin-resistant Enterococcus faecium and gentamicin-resistant Enterobacter cloacae. J Hosp Infect . 1991;;18: 211-218.
Ehrenkranz NJ, Alfonso BC.  Failure of bland soap handwash to prevent hand transfer of patient bacteria to urethral catheters. Infect Control Hosp Epidemiol . 1991;;12:654-662.
Maki DG, Alvarado CJ, Hassemer MA, Zilz MA.  Relation of the inanimate hospital environment to endemic nosocomial infections. N Engl J Med . 1982;; 307:1562-1566.
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To understand the clinical management of acute heart failure syndromes.
Accreditation Information The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians.
The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity.
Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
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For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
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Citing articles are presented as examples only. In non-demo SCM6 implementation, integration with CrossRef’s “Cited By” API will populate this tab (http://www.crossref.org/citedby.html).
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