Skip Navigation

A Multifaceted Intervention to Reduce Pandrug-Resistant Acinetobacter baumannii Colonization and Infection in 3 Intensive Care Units in a Thai Tertiary Care Center: A 3-Year Study

  1. Anucha Apisarnthanarak1,
  2. Uayporn Pinitchai2,
  3. Kanokporn Thongphubeth1,
  4. Chananart Yuekyen1,
  5. David K. Warren3,
  6. Victoria J. Fraser3, and
  7. Thammasat University Pandrug-Resistant Acinetobacter baumannii Control Group
  1. 1Division of Infectious Diseases and Infection Control, Pratumthani, Thailand
  2. 2Medical Intensive Care Unit, Thammasat University Hospital, Pratumthani, Thailand
  3. 3Division of Infectious Diseases, Washington University School of Medicine, St. Louis, Missouri
  1. Reprints or correspondence: Dr. Anucha Apisarnthanarak, Div. of Infectious Diseases, Thammasat University Hospital, Pratumthani, Thailand, 12120 (anapisarn{at}yahoo.com).
 
Next Section

Abstract

Background.We sought to determine the long-term effect of a multifaceted infection-control intervention to reduce the incidence of pandrug-resistant Acinetobacter baumannii infection in a Thai tertiary care center.

Methods.A 3-year, prospective, controlled, quasi-experimental study was conducted in medical intensive care, surgical intensive care, and coronary care units for a 1-year period before intervention (period 1), a 1-year period after intervention (period 2), and a 1-year follow-up period (period 3). The interventions in period 2 included strictly implementing contact isolation precautions and appropriate hand hygiene, active surveillance, cohorting patients who were colonized or infected with pandrug-resistant A. baumannii, and environmental cleaning with 1:100 sodium hypochlorite solution. All interventions were continued in period 3, but environmental cleaning solutions were changed to detergent and phenolic agents.

Results.Before the intervention, the rate of pandrug-resistant A. baumannii colonization and/or infection was 3.6 cases per 1000 patient-days. After the intervention, the rate of pandrug-resistant A. baumannii colonization and/or infection decreased by 66% in period 2 (to 1.2 cases per 1000 patient-days; P<.001) and by 76% in period 3 (to 0.85 cases per 1000 patient-days; P<.001). The monthly hospital antibiotic cost of treating pandrug-resistant A. baumannii colonization and/or infection and the hospitalization cost for each patient in the intervention units were also reduced by 36%–42% (P<.001) and 25%–36% (P<.001), respectively, during periods 2 and 3.

Conclusions.A multifaceted intervention featuring active surveillance and environmental cleaning resulted in sustained reductions in the rate of pandrug-resistant A. baumannii colonization and infection, the cost of antibiotic therapy, and the cost of hospitalization among intensive care unit patients in a developing country.

Pandrug-resistant (PDR) Acinetobacter baumannii has emerged as an important cause of both endemic nosocomial infections and epidemic outbreaks [1–4]. In Thailand, PDR A. baumannii has become an important cause of nosocomial infection, especially in intensive care units (ICUs) [5]. Outbreak investigations demonstrate that the main modes of transmission are environmental contamination and hand carriage by health care workers (HCWs) [6–8]. Risk factors for PDR A. baumannii include use of broad-spectrum antibiotics, prolonged hospitalization, receipt of mechanical ventilation, being hospitalized in a trauma ICU, and the use of pulsatile lavage wound irrigation [9–14]. Therefore, strict infection-control measures and the rational use of antibiotics are crucial to prevent the spread of PDR A. baumannii [2, 8]. Although infection-control interventions to prevent PDR A. baumannii transmission during an outbreak have been reported [15], no study has evaluated the long-term impact of infection-control interventions designed to limit PDR A. baumannii infection and colonization.

At Thammasat University Hospital, from 1 January 2005 through 31 December 2005, an increase in the rate of PDR A. baumannii infection and colonization was identified in the medical ICU (MICU), surgical ICU (SICU) and coronary care unit (CCU) (to 3.6 cases per 1000 patient-days). Although the increase was not statistically significant, this represented a 42% increase in the rate of PDR A. baumannii infection and colonization, compared with the rate during the previous 12 months (2.1 cases per 1000 patient-days; P=.10). During this period (1 January 2005 through 31 December 2005), cultures of samples obtained from respiratory equipment and intravenous and other fluid solutions failed to identify a common source of infection. We sought to determine the long-term effect of multifaceted infection-control interventions, featuring active surveillance cultures (ASCs) and environmental cleaning, to prevent transmission of PDR A. baumannii.

Previous SectionNext Section

Patients and Methods

Setting and patients.Thammasat University Hospital is a 500-bed university hospital located in central Thailand. There are 3 ICUs, each of which has 8 beds. These are the MICU, SICU, and CCU, each of which has ∼450 admissions per year. These ICUs are multibed open wards in which multidisciplinary teams provide patient care. There are ∼35 HCWs caring for patients in each unit. Nurses and respiratory therapists do not rotate between ICUs. The same infectious disease consultant (IDC) evaluated patients in these units in all study periods. The estimated patient-to-nurse ratio in the ICUs was 2:1. The study population consisted of all consecutive patients admitted to the 3 ICUs from 1 January 2005 through 31 December 2007. The study consisted of a 12-month baseline observation period (1 January 2005–31 December 2005; period 1), followed by a 12-month intervention period (1 January 2006–31 December 2006; period 2) and a 12-month follow-up period (1 January 2007–31 December 2007; period 3). The intervention was performed in the MICU, SICU, and CCU. During the study period, basic infection-control measures, including hand hygiene and contact precautions, were standard practice to prevent nosocomial transmission of drug-resistant microorganisms in this hospital. An antibiotic-control program was established in this hospital in July 2004 for 4 major classes of antibiotics (third-generation cephalosporins, β-lactam/β-lactamase inhibitors, glycopeptides, and carbapenems) [16]. The antibiotic-control program did not change during the study [17]. No other protocols aimed at influencing the rates of PDR A. baumannii were introduced during the study. The medical and nursing leadership of each unit and the patient-to-nurse ratios in the ICUs remained constant during the study period.

Definition and data collection.PDR A. baumannii was defined as an A. baumannii isolate that was resistant to all currently available systemic antibiotics, including cephalosporins, aztreonam, carbapenems, aminoglycosides, fluoroquinolones, and sulbactam (except polymyxin B). Bacterial isolation and antimicrobial susceptibility testing were performed in accordance with Clinical and Laboratory Standards Institute methodology [18]. Nosocomial infection was defined using Centers for Disease Control and Prevention definitions [19]. Nosocomial acquisition of PDR A. baumannii was defined as detection of this microorganism by ASC >48 h after ICU admission, following a negative ASC result obtained at ICU admission. Case patients were defined as patients with nosocomial colonization and/or infection due to PDR A. baumannii identified by clinical cultures >48 h after admission to the study ICUs. Sustained reduction was defined as a persistent reduction in any measured outcomes of interest. The antibiotic use density for inpatients was recorded as the total number of grams of the drug, and the value was converted into defined daily doses per 1000 patient-days, in accordance with the recommendations of the World Health Organization [20]. Data on the number of patient admissions and patient-days were supplied by the hospital's medical records database system.

In all units, PDR A. baumannii colonization and infection rates were prospectively tracked by the same infection-control specialist (ICS) throughout the study and were expressed as cases of PDR A. baumannii colonization and infection per 1000 patient-days. The data collected included patient demographic characteristics, underlying diseases, severity of illness (measured by Acute Physiology and Chronic Health Evaluation II [APACHE-II] score), the occurrence of PDR A. baumannii colonization and/or infection, compliance with infection-control processes (e.g., ASC and environmental cleaning), cost of antibiotics to treat PDR A. baumannii infection, and the cost of hospitalization. The use of antibiotics to treat PDR A. baumannii colonization and infection was determined by chart reviews conducted by an IDC after excluding other possible indications. The antibiotic use categories were modified from Kunin et al. [21] and were strictly observed using a checklist [16, 17]. Costs, rather than charges, were used for each patient. The cost accounting database uses a set-down allocation method to calculate costs, which include indirect, direct, and fixed costs. All patient charge codes received during the hospitalizations were recorded, and the departmental cost for each charge code was calculated on the basis of each department's actual cost components multiplied by the charges for that code, divided by the total departmental charges. Costs were summed across each department to provide total hospital costs for each hospitalization. Only hospital-associated costs were included in analysis; physician costs were not included. Antibiotic costs were calculated on the basis of the actual dosage given to the patients and were based on the purchase price to the institution, without administration costs. All costs were converted to US dollars at an exchange rate of 35 Thai baht to 1 US dollar.

Program design.During period 1 (1 January 2005–30 November 2005), an intervention team collected and analyzed baseline data; no specific intervention was performed and no routine environmental cultures were obtained, apart from basic infection-control measures. From 1 December 2005 through 31 December 2005, feedback of baseline data was given to nursing staff and physicians in all ICUs by the intervention team, and an action plan was developed. During period 2, infection-control measures included: (1) implementation of enhanced contact isolation precautions (i.e., strict adherence to hand hygiene protocol before and after patient care and donning of gowns and gloves before patient care), (2) ASCs for PDR A. baumannii, (3) cohorting patients with PDR A. baumannii in a single section of the unit, and (4) environmental cleaning with 1:100 sodium hypochlorite solution. Similar infection-control measures were continued during period 3. Hand hygiene was promoted during periods 2 and 3 using educational sessions (performed every 4 months), posters to encourage hand hygiene with alcohol gel, and monthly feedback of handwashing compliance and PDR A. baumannii colonization and infection rates. Environmental cleaning with 1:100 sodium hypochlorite solution was performed on bed rails, sinks, overbed tables, infusion pumps, and surrounding counter tops. Daily environmental cleaning with 1:100 sodium hypochlorite solution was performed during the first 6 months of period 2 and was replaced by cleaning with detergent and phenolic agents (for surface contaminated with body fluid and/or blood) until the end of period 3. Because the optimum anatomical site to screen for PDR A. baumannii carriage is not known, ASCs for PDR A. baumannii were performed using surveillance cultures of tracheal aspirates and rectal swabs (if culture of tracheal aspirate specimens had negative results) on day 0, day 7, and every week until discharge from the ICU for all patients who were admitted to the intervention units. Contact isolation was employed for all patients with results positive for PDR A. baumannii (identified either by ASC or clinical culture) and for patients who had been recently discharged from the ICU who had culture results positive for PDR A. baumannii until there was evidence of clearance (defined as 3 culture-negative specimens obtained from sites from which culture-positive specimens had previously been obtained). All basic infection-control measures (i.e., adherence to hand hygiene before and after patient care and donning of gowns and gloves before patient care) were continuously monitored using standardized observation forms during period 3. All patients in these ICUs were intubated. The intervention team included a representative from the hospital administration, an IDC, a clinical microbiologist, ICU attending physicians and chief nurses from intervention units, 2 ICSs, and a hospital epidemiologist.

Monitoring adherence to infection-control measures.Adherence to infection-control measures was prospectively monitored in all units by the same ICS throughout the study. The ICS observed housekeepers cleaning beds throughout the study, including on weekends and/or on the night shift. We noted whether environmental sites (e.g., bed rails, over-bed tables, infusion pumps, clean countertops, and soiled countertops) were cleaned and recorded the results as “cleaned (during observation),” “not cleaned (during observation),” “not applicable” (i.e., item not present), or “not observed.” Per week, the fraction of items scored as “cleaned” and “not cleaned” was calculated. Hand hygiene observations were made by the same ICS in each unit at various times of day. Hand hygiene observations began when a HCW entered the intervention unit and was observed in an activity that involved contact with a patient or their environment and ended when that HCW completed the activity. Monitored variables included hand hygiene (with soap and water or with alcohol gel) before and after contact with the patient or environment, plus donning gowns and gloves for interacting with patients who were in contact isolation.

Statistical analysis.Categorical variables were compared using the χ2 test or Fisher's exact test, as appropriate. Normally distributed continuous variables were expressed as means (±SDs). Student's t test was used to compare continuous variables. Trend analysis was performed to evaluate the overall pattern of changes on outcomes of interest over time using interrupted time series, with segmented regression analysis performed using SPSS, version 12.0 (SPSS). All tests were 2-tailed. P<.05 was considered to be statistically significant.

Previous SectionNext Section

Results

Patient demographic characteristics.There were 4071 patients enrolled during the entire study period (1363 patients in the MICU, 1462 in the SICU, and 1246 in the CCU). The mean age of the patients was 51 years (range, 15–89 years). The patient characteristics, underlying diseases, APACHE-II score, duration of hospital stay, number of admissions per unit, and number of patients who were placed on contact isolation are summarized in table 1. There were no significant differences in patient characteristics between the study periods.

Figure 1
View larger version:
Figure 1

Rates of pandrug-resistant Acinetobacter baumanii infection and colonization in 3 intensive care units. Period 1 was the baseline period (1 January 2005 through 31 December 2005), period 2 was the intervention period (1 January 2006 through 31 December 2006), and period 3 was the follow-up period (1 January 2007 through 31 December 2007).

Table 1
View larger version:
Table 1

Characteristics of patients with pandrug-resistant Acinetobacter baumanii infection and colonization in intervention intensive care units, by study period.

Active surveillance and antimicrobial use.A total of 6965 tracheal aspirate cultures and rectal swab cultures were obtained at ICU admission in all intervention units. Ninety-five pnwoercent of the patients' medical records (2578 of 2714 patients) had documentation of ASCs being ordered (in all cases, within 4 h after ICU admission). Eighty-eight percent of patients admitted to the intervention units (2388 of 2714 patients) had >1 ASC performed (326 [12%] did not have an ASC performed because of a hospital stay <24 h in duration), and 1927 (71%) had >1 ASC performed. Daily proportions of patients in the intervention units who were colonized with PDR A. baumannii ranged from 4% to 50%. The mean colonization pressure (±SD) decreased during the 3 study periods, from 0.36±0.18 patients per day in period 1 to 0.24±0.12 patients per day in period 2 (P<.001) and 0.12±0.05 patients per day in period 3 (P<.001) (table 2). Daily admission rates of patients colonized or infected with PDR A. baumannii were 0.25 patients per day in period 1, 0.20 patients per day in period 2, and 0.21 patients per day in period 3 (P=.45). The rate of PDR A. baumannii acquisition decreased from 15.9 isolates per 1000 patient-days at-risk in period 2 to 11.9 isolates per 1000 patient-days at-risk in period 3 (P=.36). There was no difference between any of the units with respect to the antimicrobial prescribing pattern throughout the study.

Table 2
View larger version:
Table 2

Patients colonized or infected with pandrug-resistant (PDR) Acinetobacter baumannii, infection-control compliance monitoring, and outcomes in intervention intensive care units.

Rate of PDR A. baumannii infection and colonization.During period 1, there were 53 cases of PDR A. baumannii colonization and infection (3.6 cases per 1000 patient-days) in all ICUs. During period 2, the rate of PDR A. baumannii colonization and infection decreased by 66% (17 cases; 1.2 cases per 1000 patient-days; P<.001). This rate was further reduced by 76% (13 cases; 0.85 cases per 1000 patient-days; P<.001) in period 3 (figure 1). Rates of PDR A. baumannii colonization and infection in individual ICUs are given in table 3. Segmented regression analysis of the PDR A. baumannii colonization and infection rates are given in table 4.

Table 3
View larger version:
Table 3

Rate of pandrug-resistant Acinetobacter baumannii infection and colonization among intervention intensive care units.

Table 4
View larger version:
Table 4

Change in rates of pandrug-resistant Acinetobacter baumannii infection and colonization in intervention intensive care units from interrupted time series analysis, with segmented regression analysis during the entire duration of the study.

Cost of surveillance culture versus the monthly cost of hospitalization and antibiotics for treatment of PDR A. baumannii infection.The total cost for ASCs was $19,862 for the entire study. The intervention resulted in a significant reduction in the total cost of antibiotics used to treat PDR A. baumannii infection and in the cost of hospitalization (table 2). Compared with the costs in period 1, the monthly hospital antibiotic costs to treat PDR A. baumannii infection and the hospitalization costs for each patient in the intervention units in periods 2 and 3 were reduced by 36%–42% (mean cost of antibiotics, $3762 vs. $1722 vs. $1278; P<.001) and 25%–36% (mean cost of hospitalization, $366 vs. $253 vs. $204; P<.001), respectively. There were no antibiotic-related cost-cutting measures introduced during the study period.

Previous SectionNext Section

Discussion

This study showed that a multifaceted infection-control intervention can dramatically decrease the long-term incidence of PDR A. baumannii infection and colonization, the hospital cost of antibiotics for treatment of PDR A. baumannii infection, and the cost of hospitalization. The change in slope without a change in intercept in period 2 versus period 1 and in period 3 versus period 2 indicates a gradual rather than a sudden decrease in PDR A. baumanii infection and colonization. This intervention was well-accepted by housekeepers and intensive care HCWs and was sustained for 2 years.

Infections caused by multidrug-resistant (MDR) A. baumannii, particularly during outbreaks, usually represent the “iceberg phenomenon” [11], in which ratios of infection to colonization range from 1:3.5 to 1:12 [15, 22, 23]. In our study, we identified an infection-to-colonization ratio of 1:2.7 in the preintervention period. This ratio was reduced to 1:4.2 during period 2 and 1:5.2 during period 3, despite ongoing admission of patients with PDR A. baumannii infection and colonization to the ICUs and only moderate rates of adherence to proper hand hygiene. This study supports the effectiveness of ASCs to help control MDR A. baumannii infection and colonization in ICUs, as has been described elsewhere [11, 24].

Survival of Acinetobacter species on environmental surfaces may be an important determinant of transmission [25]. Previous studies have reported isolation of Acinetobacter species from environmental sites in ICUs with high rates of endemic colonization or during outbreaks [26–28]. The role of environmental cleaning in controlling MDR A. baumannii has also been emphasized in previous outbreaks of MDR A. baumannii infection [15, 25, 29–31]. As a result, environmental cleaning has been emphasized as one of the important parts of an effective infection-control strategy. The rationale for using sodium hypochlorite for environmental cleaning in our study was based on the fact that (1) several studies have used 1:100 sodium hypochlorite to control MDR A. baumannii outbreaks successfully [29–33], (2) existing data suggested that cleaning floors with either detergent or disinfectant did not affect nosocomial infection rates [34], and (3) a study reported that a quaternary ammonium compound was inadequate for disinfecting bathrooms and toilets [29]. In contrast, studies have suggested that hypochlorite-based environmental cleaning can be associated with a reduced incidence of hospital-acquired Clostridium difficile infection [35–37]. Although A. baumannii does not form spores, the persistent survival of this pathogen when desiccated is partly analogous to that of C. difficile [38]. However, because of the impact of sodium hypochlorite solution on HCW's skin and hospital surfaces [39], its use was discontinued after 6 months, during period 2, after the rate of PDR A. baumannii infection decreased significantly (figure 1).

Other important infection-control measures in our study included cohorting, ASCs, enhanced contact isolation, and improvement in hand hygiene adherence. Notably, adherence to hand hygiene improved early in period 2, perhaps as a result of the Hawthorne effect, but decreased slightly during period 3, even with continuous education and feedback regarding hand hygiene and PDR A. baumannii infection rates to HCWs. Despite only moderate hand hygiene adherence rates and continuing admission of patients with PDR A. baumannii colonization and infection, the infection and colonization rate decreased significantly during period 2 and remained low during period 3. This study reemphasizes the role of multifaceted infection-control interventions (e.g., ASCs, environmental cleaning, contact isolation, and hand hygiene) to control the spread of PDR A. baumannii. The difficulty of achieving high levels of hand hygiene adherence in ICUs, which have high workloads, is consistent with the findings of previous studies [40, 41].

There are some limitations to this study. This was not a randomized trial; therefore, other unmeasured factors might have coincided with the intervention, resulting in lower infection and colonization rates. However, this bias is conservative, because we collected the data for 12 months in each period to control for possible seasonal variations, and the patients' characteristics in each period were comparable. Because all ICUs in the hospital experienced an increase in PDR A. baumannii infection and colonization rates, a comparable control ICU could not be examined. The lack of environmental cultures and of cultures of swab samples from HCWs' hands make it difficult to prove the significance of environmental contamination or hand contamination in cross-transmission of PDR A. baumannii in settings of endemicity. Because this intervention was performed at a single medical center, these results may not be applicable to other hospitals. However, the achievement of similar effects in other settings suggests that the intervention may be generalizable to other facilities [14, 25, 29–33]. Because several interventions were made simultaneously, it is difficult to know which of the specific interventions was the most effective in controlling PDR A. baumannii infection and colonization. Because the IDC responsible for the implementation of this intervention also reviewed and recorded the use of antibiotics for treatment of PDR A. baumannii infection and colonization, bias may have been introduced, but the bias is conservative, because the IDC was experienced and consistently used explicit criteria and a checklist to monitor antibiotic use. Lastly, this intervention was labor intensive, time-consuming for the ICS, and required resources for ASC.

Despite these limitations, our study has broadened the support for the efficacy of multifaceted infection-control interventions to control PDR A. baumannii infection in a resource-limited setting. Because treatment of PDR A. baumannii infection can be associated with high morbidity, mortality, and costs, these basic infection-control strategies remain key to the control of PDR A. baumannii infection in developing countries.

Previous SectionNext Section

Acknowledgments

We thank all medical intensive care unit, surgical intensive care unit, and coronary care unit staff and the Thammasat University Pandrug Resistant Acinetobacter baumannii Control Group for their dedication and commitment to reducing the incidence of pandrug-resistant A. baumannii throughout the study period.

Financial support.Infectious Diseases and Hospital Epidemiology Research Unit at Thammasat University (Pratumthani, Thailand).

Potential conflicts of interest.D.K.W. has received research funding from 3M Healthcare and Sage Products; has served as a consultant for 3M Healthcare, Enturia, and NovaBay Pharmaceuticals; and has received speaker honoraria from Cook. All other authors: no conflicts.

  • Received March 18, 2008.
  • Accepted May 19, 2008.
Previous Section
 

references

  1. ↵
    1. Hsueh PR,
    2. Teng LJ,
    3. Chen CY,
    4. et al
    . Pandrug-resistant Acinetobacter baumannii causing nosocomial infections in a university hospital, Taiwan. Emerg Infect Dis 2002;8:827-32.
    MedlineWeb of Science
  2. ↵
    1. Kuo LC,
    2. Yu CJ,
    3. Lee LN,
    4. et al
    . Clinical features of pandrug-resistant Acinetobacter baumannii bacteremia at a university hospital in Taiwan. J Formos Med Assoc 2003;102:601-6.
    MedlineWeb of Science
    1. Falagas ME,
    2. Bliziotis IA
    . Pandrug-resistant Gram-negative bacteria: the dawn of the post-antibiotic era? Int J Antimicrob Agents 2007;29:630-6.
    CrossRefMedlineWeb of Science
  4. ↵
    1. Falagas ME,
    2. Rafailidis PI
    . Attributable mortality of Acinetobacter baumannii: no longer a controversial issue. Crit Care 2007;11:134.
    CrossRefMedline
  5. ↵
    1. Dejsirilert S,
    2. Apisarnthanarak A,
    3. Kitphati R,
    4. et al
    . Program and abstracts of the 9th Western Pacific Congress on Chemotherapy and Infectious Diseases (Bangkok). Bangkok: Medinfo GD; 2004. The status of antimicrobial resistance in Thailand among gram-negative pathogens in bloodstream infections: NARST data, 2000–2003 [abstract FP-A-3]; p. 185.
  6. ↵
    1. Lortholary O,
    2. Fagon JY,
    3. Hoi AB,
    4. et al
    . Nosocomial acquisition of multiresistant Acinetobacter baumannii: risk factors and prognosis. Clin Infect Dis 1995;20:790-6.
    Abstract/FREE Full Text
    1. Koeleman JG,
    2. Parlevliet GA,
    3. Dijkshoorn L,
    4. Savelkoul PH,
    5. Vandenbroucke-Grauls CM
    . Nosocomial outbreak of multi-resistant Acinetobacter baumannii on a surgical ward: epidemiology and risk factors for acquisition. J Hosp Infect 1997;37:113-23.
    CrossRefMedlineWeb of Science
  8. ↵
    1. Wang SH,
    2. Sheng WH,
    3. Chang YY,
    4. et al
    . Healthcare-associated outbreak due to pan-drug resistant Acinetobacter baumannii in a surgical intensive care unit. J Hosp Infect 2003;53:97-102.
    CrossRefMedlineWeb of Science
  9. ↵
    1. El Shafie SS,
    2. Alishaq M,
    3. Leni Garcia M
    . Investigation of an outbreak of multidrug-resistant Acinetobacter baumannii in trauma intensive care unit. J Hosp Infect 2004;56:101-5.
    CrossRefMedlineWeb of Science
    1. Villers D,
    2. Espaze E,
    3. Coste-Burel M,
    4. et al
    . Nosocomial Acinetobacter baumannii infections: microbiological and clinical epidemiology. Ann Intern Med 1998;129:182-9.
    Abstract/FREE Full Text
  11. ↵
    1. Abbo A,
    2. Navon-Venezia S,
    3. Hammer-Muntz O,
    4. et al
    . Multidrug-resistant Acinetobacter baumannii. Emerg Infect Dis 2005;11:22-9.
    MedlineWeb of Science
    1. Maragakis LL,
    2. Cosgrove SE,
    3. Song X,
    4. et al
    . An outbreak of multidrug-resistant Acinetobacter baumannii associated with pulsatile lavage wound treatment. JAMA 2004;292:3006-11.
    Abstract/FREE Full Text
    1. Husni RN,
    2. Goldstein LS,
    3. Arroliga AC,
    4. et al
    . Risk factors for an outbreak of multi-drug-resistant Acinetobacter nosocomial pneumonia among intubated patients. Chest 1999;115:1378-82.
    Abstract/FREE Full Text
  14. ↵
    1. Mulin B,
    2. Talon D,
    3. Viel JF,
    4. et al
    . Risk factors for nosocomial colonization with multiresistant Acinetobacter baumannii. Eur J Clin Microbiol Infect Dis 1995;14:569-76.
    CrossRefMedlineWeb of Science
  15. ↵
    1. Chan PC,
    2. Huang LM,
    3. Lin HC,
    4. et al
    . Control of an outbreak of pandrug-resistant Acinetobacter baumannii colonization and infection in a neonatal intensive care unit. Infect Control Hosp Epidemiol 2007;28:423-9.
    CrossRefMedlineWeb of Science
  16. ↵
    1. Apisarnthanarak A,
    2. Danchaivijitr S,
    3. Khawcharoenporn T,
    4. et al
    . Effectiveness of education and an antibiotic-control program in a tertiary care hospital in Thailand. Clin Infect Dis 2006;42:768-75.
    Abstract/FREE Full Text
  17. ↵
    1. Apisarnthanarak A,
    2. Srichomkwun P,
    3. Sutepvarnon A,
    4. Bailey TC,
    5. Fraser VJ
    . The long-term outcomes of an antibiotic control program with and without education. Clin Infect Dis 2007;45:1245-7.
    FREE Full Text
  18. ↵
    1. Clinical and Laboratory Standards Institute (CLSI)
    . Performance standards for antimicrobial susceptibility testing: seventeenth informational supplement. Wayne, PA: CLSI; 2007. p. 100-17.
  19. ↵
    1. Mayhall CG
    1. Horan TC,
    2. Gaynes RP
    . Surveillance of nosocomial infections. In: Mayhall CG, editor. Hospital epidemiology and infection control. 3rd ed. Philadelphia: Lippincott Williams & Wilkins; 2004. p. 1659-1702.
  20. ↵
    1. Maxwell M,
    2. Heaney D,
    3. Howie JG,
    4. Noble S
    . General practice fund holding: observations on prescribing patterns and costs during the defined daily dose method. BMJ 1993;307:1190-4.
    Abstract/FREE Full Text
  21. ↵
    1. Kunin CM,
    2. Tupasi T,
    3. Craig WA
    . Use of antibiotics; a brief exposition of the problem and some tentative solutions. Ann Intern Med 1973;79:555-60.
    Abstract/FREE Full Text
  22. ↵
    1. Schloesser RL,
    2. Laufkoetter EA,
    3. Lehners T,
    4. Mietens C
    . An outbreak of Acinetobacter calcoaceticus infection in a neonatal care unit. Infection 1990;18:230-3.
    CrossRefMedlineWeb of Science
  23. ↵
    1. McDonald LC,
    2. Walker M,
    3. Carson L,
    4. et al
    . Outbreak of Acinetobacter spp. bloodstream infections in a nursery associated with contaminated aerosols and air conditioners. Pediatr Infect Dis J 1998;17:716-22.
    CrossRefMedlineWeb of Science
  24. ↵
    1. Webster CA,
    2. Crowe M,
    3. Humphreys H,
    4. Towner KJ
    . Surveillance of an adult intensive care unit for long-term persistence of a multi-resistant strain of Acinetobacter baumannii. Eur J Clin Microbiol Infect Dis 1998;17:171-6.
    MedlineWeb of Science
  25. ↵
    1. Wilks M,
    2. Wilson A,
    3. Warwick S,
    4. et al
    . Control of an outbreak of multidrug-resistant Acinetobacter baumannii-calcoaceticus colonization and infection in an intensive care unit (ICU) without closing the ICU or placing patients in isolation. Infect Control Hosp Epidemiol 2006;27:654-8.
    CrossRefMedlineWeb of Science
  26. ↵
    1. Villegas MV,
    2. Hartstein AI
    . Acinetobacter outbreaks, 1977–2000. Infect Control Hosp Epidemiol 2003;24:284-95.
    CrossRefMedlineWeb of Science
    1. Houang ET,
    2. Chu YW,
    3. Leung CM,
    4. et al
    . Epidemiology and infection control implications of Acinetobacter spp. in Hong Kong. J Clin Microbiol 2001;39:228-34.
    Abstract/FREE Full Text
  28. ↵
    1. Catalano M,
    2. Quelle LS,
    3. Jeric PE,
    4. Di Martino A,
    5. Maimone SM
    . Survival of Acinetobacter baumannii on bed rails during an outbreak and during sporadic cases. J Hosp Infect 1999;42:27-35.
    CrossRefMedlineWeb of Science
  29. ↵
    1. Denton M,
    2. Wilcox MH,
    3. Parnell P,
    4. et al
    . Role of environmental cleaning in controlling an outbreak of Acinetobacter baumannii on a neurosurgical intensive care unit. Intensive Crit Care Nurs 2005;21:94-8.
    CrossRefMedline
    1. Denton M,
    2. Wilcox MH,
    3. Parnell P,
    4. et al
    . Role of environmental cleaning in controlling an outbreak of Acinetobacter baumannii on a neurosurgical intensive care unit. J Hosp Infect 2004;56:106-10.
    CrossRefMedlineWeb of Science
  31. ↵
    1. Pimental JD,
    2. Low J,
    3. Styles K,
    4. Harris OC,
    5. Hughes A,
    6. Athan E
    . Control of an outbreak of multi-drug resistant Acinetobacter baumannii in an intensive care unit and a surgical unit. J Hosp Infect 2005;59:249-53.
    CrossRefMedlineWeb of Science
    1. Aygün G,
    2. Demirkiran O,
    3. Utku T,
    4. et al
    . Environmental contamination during a carbapenem-resistant Acinetobacter baumannii outbreak in an intensive care unit. J Hosp Infect 2002;52:259-62.
    CrossRefMedlineWeb of Science
  33. ↵
    1. Das I,
    2. Lambert P,
    3. Hill D,
    4. Noy M,
    5. Bion J,
    6. Elliott T
    . Carbapenem-resistant Acinetobacter and role of curtains in an outbreak in intensive care units. J Hosp Infect 2002;50:110-4.
    CrossRefMedlineWeb of Science
  34. ↵
    1. Danforth D,
    2. Nicolle LE,
    3. Hume K,
    4. Alfieri N,
    5. Sims H
    . Nosocomial infections on nursing units with floors cleaned with a disinfectant compared with detergent. J Hosp Infect 1987;10:229-35.
    CrossRefMedlineWeb of Science
  35. ↵
    1. Mayfield JL,
    2. Leet T,
    3. Miller J,
    4. Mundy LM
    . Environmental control to reduce transmission of Clostridium difficile. Clin Infect Dis 2000;31:995-1000.
    Abstract/FREE Full Text
    1. Apisarnthanarak A,
    2. Zack JE,
    3. Mayfield JL,
    4. et al
    . Effectiveness of environmental and infection control programs to reduce transmission of Clostridium difficile. Clin Infect Dis 2004;39:601-2.
    FREE Full Text
  37. ↵
    1. Wilcox MH,
    2. Fawley WN,
    3. Wigglesworth N,
    4. Parnell P,
    5. Verity P,
    6. Freeman J
    . Comparison of the effect of detergent versus hypochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection. J Hosp Infect 2003;54:109-14.
    CrossRefMedlineWeb of Science
  38. ↵
    1. Jawad A,
    2. Seifert H,
    3. Snelling AM,
    4. Heritage J,
    5. Hawkey PM
    . Survival of Acinetobacter baumannii on dry surfaces: comparison of outbreak and sporadic isolates. J Clin Microbiol 1998;36:1938-41.
    Abstract/FREE Full Text
  39. ↵
    1. Rutala WA,
    2. Weber DJ
    . Disinfection and sterilization in health care facilities: what clinicians need to know. Clin Infect Dis 2004;39:702-9.
    Abstract/FREE Full Text
  40. ↵
    1. Boyce JM,
    2. Pittet D
    . Guideline for hand hygiene in health-care settings. Recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Society for Healthcare Epidemiology of America/Association for Professionals in Infection Control/Infectious Diseases Society of America. MMWR Recomm Rep 2002;51(RR-16):1-45. CE1-4.
    Medline
  41. ↵
    1. Pittet D,
    2. Simon A,
    3. Hugonnet S,
    4. Pessoa-Silva CL,
    5. Sauvan V,
    6. Perneger TV
    . Hand hygiene among physicians: performance, beliefs, and perceptions. Ann Intern Med 2004;141:1-8.
    Abstract/FREE Full Text
| Table of Contents

This Article

  1. Clin Infect Dis. (2008) 47 (6): 760-767. doi: 10.1086/591134
  1. AbstractFree
  2. » Full Text (HTML)Free
  3. Full Text (PDF)Free

Classifications

Share

  1. Email this article

Navigate This Article

Current Issue

  1. March 1, 2012 54 (5)
  1. Clinical Infectious Diseases
  1. Alert me to new issues

Most