Epidemiology, Prevalence, and Sites of Infections in Intensive Care Units

Michael Richards; Karin Thursky; Kirsty Buising

doi:10.1055/s-2003-37913

Seminars in Respiratory and Critical Care Medicine, Table of Contents

Semin Respir Crit Care Med 2003; 24(1): 003-022
DOI: 10.1055/s-2003-37913

Epidemiology, Prevalence, and Sites of Infections in Intensive Care Units

Michael Richards^1,2 , Karin Thursky² , Kirsty Buising²

¹VICNISS Coordinating Centre for Surveillance of Hospital Acquired Infection, North Melbourne, Victoria, Australia
²Victorian Infectious Diseases Service, Royal Melbourne Hospital, Parkville, Victoria, Australia

Abstract

ABSTRACT

Patients in intensive care units (ICUs) have a higher risk of acquiring hospital-associated infections than those in non-critical care areas. ICUs are sites of considerable broad-spectrum antibiotic use, and antibiotic-resistant pathogens are frequent. Bloodstream infections (BSIs), pneumonias, and urinary tract infections (UTIs) are the most common hospital-acquired infections and are most often associated with the use of invasive devices. They differ in importance in different types of ICUs. Coagulase-negative staphylococcus BSIs have recently increased in frequency, and enterococci have been as frequently reported as Staphylococcus aureus as causing BSIs in increasing numbers of U.S. ICUs. Fungal urinary tract sepsis has also increased. Device-associated infection rates represent the most useful surveillance rates for comparison between units and over time, but they differ considerably between ICU types. Outbreaks are common in ICUs. Recently, gram-negative bacilli have been reported more frequently than gram-positives in this setting, especially in NICUs. Considerable crude mortality and major costs are associated with these infections, but controversy persists over the degree of mortality attributable to them.

KEYWORDS

Cross infection - epidemiology - intensive care units

Full Text

References

REFERENCES

1 Weinstein R A. Nosocomial infection update. Emerg Infect Dis . 1998; 4 416-420
2 Kohn L, Corrigan J, Donaldson M. To err is human: building a safer health system. Washington, DC: Institute of Medicine 1999
3 Haley R W, Culver D H, White J W. The efficacy of infection surveillance and control programs in preventing nosocomial infections in US hospitals. Am J Epidemiol . 1985; 121 182-205
4 Archibald L K, Manning M L, Bell L M, Banerjee S, Jarvis W R. Patient density, nurse-to-patient ratio and nosocomial infection risk in a pediatric cardiac intensive care unit. Pediatr Infect Dis J . 1997; 16 1045-1048
5 Donowitz L G, Wenzel R P, Hoyt J W. High risk of hospital-acquired infection in the ICU patient. Crit Care Med . 1982; 10 355-357
6 Albrich W C, Angstwurm M, Bader L, Gartner R. Drug resistance in intensive care units. Infection . 1999; 27 (suppl 2) S19-S23
7 Alberti C, Brun-Buisson C, Burchardi H. Epidemiology of sepsis and infection in ICU patients from an international multicentre cohort study. Intensive Care Med . 2002; 28 108-121
8 Vincent J L, Bihari D J, Suter P M. The prevalence of nosocomial infection in intensive care units in Europe. Results of the European Prevalence of Infection in Intensive Care (EPIC) Study. EPIC International Advisory Committee. JAMA . 1995; 274 639-644
9 Richards M J, Edwards J R, Culver D H, Gaynes R P. Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol . 2000; 21 510-515
10 Fridkin S K, Welbel S F, Weinstein R A. Magnitude and prevention of nosocomial infections in the intensive care unit. Infect Dis Clin North Am . 1997; 11 479-496
11 Fridkin S K, Gaynes R P. Antimicrobial resistance in intensive care units. Clin Chest Med . 1999; 20 303-316
12 Jarvis W R, Edwards J R, Culver D H. Nosocomial infection rates in adult and pediatric intensive care units in the United States. National Nosocomial Infections Surveillance System. Am J Med . 1991; 91(3B) 185S-191S
13 Richards M J, Edwards J R, Culver D H, Gaynes R P. Nosocomial infections in pediatric intensive care units in the United States. National Nosocomial Infections Surveillance System. Pediatrics . 1999; 103 e39
14 Richards M J, Edwards J R, Culver D H, Gaynes R P. Nosocomial infections in medical intensive care units in the United States. National Nosocomial Infections Surveillance System. Crit Care Med . 1999; 27 887-892
15 Monitoring hospital-acquired infections to promote patient safety-United States, 1990-1999. Morb Mortal Wkly Rep . 2000; 49 149-153
16 NNIS Semiannual Report Atlanta: CDC, U.S Department of Health and Human Services 2000
17 National Nosocomial Infections Surveillance (NNIS) System report, data summary from October 1986-April 1998, issued June 1998. Am J Infect Control . 1998; 26 522-533
18 Wallace W C, Cinat M E, Nastanski F, Gornick W B, Wilson S E. New epidemiology for postoperative nosocomial infections. Am Surg . 2000; 66 874-878
19 National Nosocomial Infections Surveillance (NNIS) System Report, Data Summary from January 1992-June 2001, issued August 2001. Am J Infect Control . 2001; 29 404-421
20 Grohskopf L A, Sinkowitz-Cochran R L, Garrett D O. A national point-prevalence survey of pediatric intensive care unit-acquired infections in the United States. J Pediatr . 2002; 140 432-438
21 Waggoner-Fountain L A, Donowitz L G. Infection in the newborn. In: Wenzel RP, ed. Prevention and Control of Nosocomial Infections 3rd ed. Pennsylvania: Williams & Wilkins 1997: 1025-1027
22 Goldmann D A, Leclair J, Macone A. Bacterial colonization of neonates admitted to an intensive care environment. J Pediatr . 1978; 93 288-293
23 Cronin W A, Germanson T P, Donowitz L G. Intravascular catheter colonization and related bloodstream infection in critically ill neonates. Infect Control Hosp Epidemiol . 1990; 11 301-308
24 Gaynes R P. Surveillance of nosocomial infections: a fundamental ingredient for quality. Infect Control Hosp Epidemiol . 1997; 18 475-478
25 Gaynes R P, Edwards J R, Jarvis W R. Nosocomial infections among neonates in high-risk nurseries in the United States. Pediatrics . 1996; 98 357-361
26 Papia G, Louie M, Tralla A, Johnson C, Collins V, Simor A E. Screening high-risk patients for methicillin-resistant Staphylococcus aureus on admission to the hospital: is it cost effective?. Infect Control Hosp Epidemiol . 1999; 20 473-477
27 Caplan E S. Nosocomial infections found to be major cause of death after trauma. Hosp Infect Control . 1980; 7 102-103
28 Caplan E S, Hoyt N J. Identification and treatment of infections in multiply traumatized patients. Am J Med . 1985; 79(1A) 68-76
29 Bell L M, Baker M D, Beatty D, Taylor L. Infections in severely traumatized children. J Pediatr Surg . 1992; 27 1394-1398
30 Miller Jr H E, Caplan E S. Nosocomial Haemophilus pneumonia in patients with severe trauma. Surg Gynecol Obstet . 1984; 159 153-156
31 Campbell W, Hendrix E, Schwalbe R, Fattom A, Edelman R. Head-injured patients who are nasal carriers of Staphylococcus aureus are at high risk for Staphylococcus aureus pneumonia. Crit Care Med . 1999; 27 798-801
32 Wurtz R, Karajovic M, Dacumos E, Jovanovic B, Hanumadass M. Nosocomial infections in a burn intensive care unit. Burns . 1995; 21 181-184
33 Appelgren P, Bjornhagen V, Bragderyd K, Jonsson C E, Ransjo U. A prospective study of infections in burn patients. Burns . 2002; 28 39-46
34 Taylor G D, Kibsey P, Kirkland T, Burroughs E, Tredget E. Predominance of staphylococcal organisms in infections occurring in a burns intensive care unit. Burns . 1992; 18 332-335
35 Wenzel R P, Thompson R L, Landry S M. Hospital-acquired infections in intensive care unit patients: an overview with emphasis on epidemics. Infect Control . 1983; 4 371-375
36 Manson W L, Pernot P C, Fidler V, Sauer E W, Klasen H J. Colonization of burns and the duration of hospital stay of severely burned patients. J Hosp Infect . 1992; 22 55-63
37 Kluytmans J A. Surgical infections including burns. In: Wenzel RP, ed. Prevention and Control of Nosocomial Infections 3rd ed. Pennsylvania: Williams & Wilkins 1997
38 Kaushik R, Kumar S, Sharma R, Lal P. Bacteriology of burn wounds-the first three years in a new burn unit at the Medical College Chandigarh. Burns . 2001; 27 595-597
39 Song W, Lee K M, Kang H J, Shin D H, Kim D K. Microbiologic aspects of predominant bacteria isolated from the burn patients in Korea. Burns . 2001; 27 136-139
40 Lari A R, Alaghehbandan R. Nosocomial infections in an Iranian burn care center. Burns . 2000; 26 737-740
41 Garcia Bernal J F, Torrero V, Regalado J, Gabilondo F J. Bacteriology in burn patients undergoing mechanical ventilation. Burns . 2000; 26 731-736
42 Brooks A, Ekleberry A, McMahon J. Evaluation of clinical practice guidelines on outcome of infection in medical intensive care unit patients. Infect Dis Clin Pract . 1999; 8 97-106
43 Eggimann P, Harbarth S, Constantin M N, Touveneau S, Chevrolet J C, Pittet D. Impact of a prevention strategy targeted at vascular-access care on incidence of infections acquired in intensive care. Lancet . 2000; 355 1864-1868
44 Richards M J, Edwards J R, Culver D H, Gaynes R P. Nosocomial infections in coronary care units in the United States. National Nosocomial Infections Surveillance System. Am J Cardiol . 1998; 82 789-793
45 Haley R W, Tenney J H, Lindsey J O, Garner J S, Bennett J V. How frequent are outbreaks of nosocomial infection in community hospitals?. Infect Control . 1985; 6 233-236
46 Wendt C, Herwaldt L A. Epidemics: identification and management. In: Wenzel RP, ed. Prevention and Control of Nosocomial Infections 3rd ed. Pennsylvania: Williams & Wilkins 1997: 175-179
47 Damjanovic V, van Saene K H. Outbreaks of infection in neonatal intensive care units (NICU). J Hosp Infect . 1997; 35 237-244
48 Dennesen P J, Bonten M J, Weinstein R A. Multiresistant bacteria as a hospital epidemic problem. Ann Med . 1998; 30 176-185
49 Guideline for prevention of nosocomial pneumonia: Centers for Disease Control and Prevention. Respir Care . 1994; 39 1191-1236
50 D'Amico R, Pifferi S, Leonetti C, Torri V, Tinazzi A, Liberati A. Effectiveness of antibiotic prophylaxis in critically ill adult patients: systematic review of randomised controlled trials. BMJ . 1998; 316 1275-1285
51 Sanchez Garcia M, Cambronero Galache A J, Lopez D iaz. Effectiveness and cost of selective decontamination of the digestive tract in critically ill intubated patients: a randomized, double-blind, placebo-controlled, multicenter trial. Am J Respir Crit Care Med . 1998; 158 908-916
52 Vandenbroucke-Grauls C M, Vandenbroucke J P. Effect of selective decontamination of the digestive tract on respiratory tract infections and mortality in the intensive care unit. Lancet . 1991; 338 859-862
53 Rello J, Ausina V, Ricart M. Risk factors for infection by Pseudomonas aeruginosa in patients with ventilator-associated pneumonia. Intensive Care Med . 1994; 20 193-198
54 Prod'hom G, Leuenberger P, Koerfer J. Nosocomial pneumonia in mechanically ventilated patients receiving antacid, ranitidine, or sucralfate as prophylaxis for stress ulcer: a randomized controlled trial. Ann Intern Med . 1994; 120 653-662
55 Markowicz P, Wolff M, Djedaini K. Multicenter prospective study of ventilator-associated pneumonia during acute respiratory distress syndrome: incidence, prognosis, and risk factors. ARDS Study Group. Am J Respir Crit Care Med . 2000; 161 1942-1948
56 Messori A, Trippoli S, Vaiani M, Gorini M, Corrado A. Bleeding and pneumonia in intensive care patients given ranitidine and sucralfate for prevention of stress ulcer: meta-analysis of randomised controlled trials. BMJ . 2000; 321 1103-1106
57 Cook D, Randolph A, Kernerman P. Central venous catheter replacement strategies: a systematic review of the literature. Crit Care Med . 1997; 25 1417-1424
58 Garibaldi R A, Burke J P, Britt M R, Miller M A, Smith C B. Meatal colonization and catheter-associated bacteriuria. N Engl J Med . 1980; 303 316-318
59 Garibaldi R A, Burke J P, Dickman M L, Smith C B. Factors predisposing to bacteriuria during indwelling urethral catheterization. N Engl J Med . 1974; 291 215-219
60 Rouby J J, Laurent P, Gosnach M. Risk factors and clinical relevance of nosocomial maxillary sinusitis in the critically ill. Am J Respir Crit Care Med . 1994; 150 776-783
61 Holzapfel L, Chevret S, Madinier G. Influence of long-term oro- or nasotracheal intubation on nosocomial maxillary sinusitis and pneumonia: results of a prospective, randomized, clinical trial. Crit Care Med . 1993; 21 1132-1138
62 Fagon J Y, Novara A, Stephan F, Girou E, Safar M. Mortality attributable to nosocomial infections in the ICU. Infect Control Hosp Epidemiol . 1994; 15 428-434
63 Escolano S, Golmard J L, Korinek A M, Mallet A. A multi-state model for evolution of intensive care unit patients: prediction of nosocomial infections and deaths. Stat Med . 2000; 19 3465-3482
64 Stephan F, Cheffi A, Bonnet F. Nosocomial infections and outcome of critically ill elderly patients after surgery. Anesthesiology . 2001; 94 407-414
65 Craven D E, Kunches L M, Lichtenberg D A. Nosocomial infection and fatality in medical and surgical intensive care unit patients. Arch Intern Med . 1988; 148 1161-1168
66 Constantini M, Donisi P M, Turrin M G. Hospital acquired infectious surveillance and control in intensive care services: results of an incidence study. Eur J Epidemiol . 1987; 3 347-355
67 Fagon J Y, Chastre J, Vuagnat A, Trouillet J L, Novara A, Gibert C. Nosocomial pneumonia and mortality among patients in intensive care units. JAMA . 1996; 275 866-869
68 Cook D. Ventilator associated pneumonia: perspectives on the burden of illness. Intensive Care Med . 2000; 26(suppl 1) S31-S37
69 Bercault N, Boulain T. Mortality rate attributable to ventilator-associated nosocomial pneumonia in an adult intensive care unit: a prospective case-control study. Crit Care Med . 2001; 29 2303-2309
70 Koss W G, Khalili T M, Lemus J F, Chelly M M, Margulies D R, Shabot M M. Nosocomial pneumonia is not prevented by protective contact isolation in the surgical intensive care unit. Am Surg . 2001; 67 1140-1144
71 Kollef M H, Silver P, Murphy D M, Trovillion E. The effect of late-onset ventilator-associated pneumonia in determining patient mortality. Chest . 1995; 108 1655-1662
72 Baker A M, Meredith J W, Haponik E F. Pneumonia in intubated trauma patients: microbiology and outcomes. Am J Respir Crit Care Med . 1996; 153 343-349
73 Mainous M R, Lipsett P A, O'Brien M. Enterococcal bacteremia in the surgical intensive care unit: does vancomycin resistance affect mortality?. <~>The Johns Hopkins SICU Study Group. Arch Surg . 1997; 132 76-81
74 Garrouste-Orgeas M, Chevret S, Mainardi J L, Timsit J F, Misset B, Carlet J. A one-year prospective study of nosocomial bacteraemia in ICU and non-ICU patients and its impact on patient outcome. J Hosp Infect . 2000; 44 206-213
75 Rello J, Ricart M, Mirelis B. Nosocomial bacteremia in a medical-surgical intensive care unit: epidemiologic characteristics and factors influencing mortality in 111 episodes. Intens Care Med . 1994; 20 94-98
76 Soufir L, Timsit J F, Mahe C, Carlet J, Regnier B, Chevret S. Attributable morbidity and mortality of catheter-related septicemia in critically ill patients: a matched, risk-adjusted, cohort study. Infect Control Hosp Epidemiol . 1999; 20 396-401
77 Warren D K, Zack J E, Elward A M, Cox M J, Fraser V J. Nosocomial primary bloodstream infections in intensive care unit patients in a nonteaching community medical center: a 21-month prospective study. Clin Infect Dis . 2001; 33 1329-1335
78 Digiovine B, Chenoweth C, Watts C, Higgins M. The attributable mortality and costs of primary nosocomial bloodstream infections in the intensive care unit. Am J Respir Crit Care Med . 1999; 160 976-981
79 Ibelings M M, Bruining H A. Methicillin-resistant Staphylococcus aureus: acquisition and risk of death in patients in the intensive care unit. Eur J Surg . 1998; 164 411-418
80 Blot S, Vandewoude K, De Bacquer D, Colardyn F. Nosocomial bacteremia caused by antibiotic-resistant gram-negative bacteria in critically ill patients: clinical outcome and length of hospitalization. Clin Infect Dis . 2002; 34 1600-1606
81 Rello J, Rue M, Jubert P. Survival in patients with nosocomial pneumonia: impact of the severity of illness and the etiologic agent. Crit Care Med . 1997; 25 1862-1867
82 Garcia-Garmendia J L, Ortiz-Leyba C, Garnacho-Montero J, Jimenez-Jimenez F J, Monterrubio-Villar J, Gili-Miner M. Mortality and the increase in length of stay attributable to the acquisition of Acinetobacter in critically ill patients. Crit Care Med . 1999; 27 1794-1799
83 Chen Y C, Lin S F, Liu C J, Jiang D D, Yang P C, Chang S C. Risk factors for ICU mortality in critically ill patients. J Formos Med Assoc . 2001; 100 656-661
84 Pittet D, Tarara D, Wenzel R P. Nosocomial bloodstream infection in critically ill patients: excess length of stay, extra costs, and attributable mortality. JAMA . 1994; 271 1598-1601
85 Kollef M H, Sherman G, Ward S, Fraser V J. Inadequate antimicrobial treatment of infections: a risk factor for hospital mortality among critically ill patients. Chest . 1999; 115 462-474
86 Chaix C, Durand-Zaleski I, Alberti C, Brun-Buisson C. Control of endemic methicillin-resistant Staphylococcus aureus: a cost-benefit analysis in an intensive care unit. JAMA . 1999; 282 1745-1751
87 Saulnier F F, Hubert H, Onimus T M. Assessing excess nurse work load generated by multiresistant nosocomial bacteria in intensive care. Infect Control Hosp Epidemiol . 2001; 22 273-278
88 Phillips G D, Chong C, Gordon P J. Nurse staffing in intensive care units. Anaesth Intensive Care . 1983; 11 118-124
89 Fridkin S K, Pear S M, Williamson T H, Galgiani J N, Jarvis W R. The role of understaffing in central venous catheter- associated bloodstream infections. Infect Control Hosp Epidemiol . 1996; 17 150-158
90 Robert J, Fridkin S K, Blumberg H M. The influence of the composition of the nursing staff on primary bloodstream infection rates in a surgical intensive care unit. Infect Control Hosp Epidemiol . 2000; 21 12-17
91 Tarnow-Mordi W O, Hau C, Warden A, Shearer A J. Hospital mortality in relation to staff workload: a 4-year study in an adult intensive care unit. Lancet . 2000; 356 185-189
92 Vicca A F. Nursing staff workload as a determinant of methicillin-resistant Staphylococcus aureus spread in an adult intensive therapy unit. J Hosp Infect . 1999; 43 109-113
93 Sherertz R J, Ely E W, Westbrook D M. Education of physicians-in-training can decrease the risk for vascular catheter infection. Ann Intern Med . 2000; 132 641-648
94 Monnet D L, Archibald L K, Phillips L, Tenover F C, McGowan Jr E J, Gaynes R P. Antimicrobial use and resistance in eight US hospitals: complexities of analysis and modeling. Intensive Care Antimicrobial Resistance Epidemiology Project and National Nosocomial Infections Surveillance System Hospitals. Infect Control Hosp Epidemiol . 1998; 19(suppl 4) 388-394
95 Niederman M S. Impact of antibiotic resistance on clinical outcomes and the cost of care. Crit Care Med . 2001; 29 N114-N120
96 Dupont H, Mentec H, Sollet J P, Bleichner G. Impact of appropriateness of initial antibiotic therapy on the outcome of ventilator-associated pneumonia. Intensive Care Med . 2001; 27 355-362
97 Raymond D P, Pelletier S J, Crabtree T D. Impact of a rotating empiric antibiotic schedule on infectious mortality in an intensive care unit. Crit Care Med . 2001; 29 1101-1108
98 Haley R W, Morgan W M, Culver D H. Update from the SENIC project: hospital infection control: recent progress and opportunities under prospective payment. Am J Infect Control . 1985; 13 97-108
99 Emori T G, Edwards J R, Culver D H. Accuracy of reporting nosocomial infections in intensive care unit patients to the National Nosocomial Infections Surveillance System: a pilot study [published erratum appears in Infect Control Hosp Epidemiol 1998 Jul;19:479]. Infect Control Hosp Epidemiol . 1998; 19 308-316
99a Bouletreau A, Dettenkofer M, Forster D H. Comparison of effectiveness and required time of two surveillance methods in intensive care patients. J Hosp Infect . 1999; 41 281-289
100 Glupczynski Y. Usefulness of bacteriological surveillance cultures for monitoring infection in hospitalized patients: a critical reappraisal. Acta Clin Belg . 2001; 56 38-45
101 Girou E, Pujade G, Legrand P, Cizeau F, Brun-Buisson C. Selective screening of carriers for control of methicillin-resistant Staphylococcus aureus (MRSA) in high-risk hospital areas with a high level of endemic MRSA. Clin Infect Dis . 1998; 27 543-550
102 Villari P, Iacuzio L, Torre I, Scarcella A. Molecular epidemiology as an effective tool in the surveillance of infections in the neonatal intensive care unit. J Infect . 1998; 37 274-281
103 Intensive Care Antimicrobial Resistance Epidemiology (ICARE) Surveillance Report, data summary from January 1996 through December 1997; a report from the National Nosocomial Infections Surveillance (NNIS) System. Am J Infect Control . 1999; 27 279-284
104 Fierobe L, Lucet J C, Decre D. An outbreak of imipenem-resistant Acinetobacter baumannii in critically ill surgical patients. Infect Control Hosp Epidemiol . 2001; 22 35-40
105 Simor A E, Lee M, Vearncombe M. An outbreak due to multiresistant Acinetobacter baumannii in a burn unit: risk factors for acquisition and management. Infect Control Hosp Epidemiol . 2002; 23 261-267
106 Debast S B, Meis J F, Melchers W J, Hoogkamp-Korstanje J A, Voss A. Use of interrepeat PCR fingerprinting to investigate an Acinetobacter baumannii outbreak in an intensive care unit. Scand J Infect Dis . 1996; 28 577-581
107 D'Agata E M, Thayer V, Schaffner W. An outbreak of Acinetobacter baumannii: the importance of cross-transmission. Infect Control Hosp Epidemiol . 2000; 21 588-591
108 Mah M W, Memish Z A, Cunningham G, Bannatyne R M. Outbreak of Acinetobacter baumannii in an intensive care unit associated with tracheostomy. Am J Infect Control . 2001; 29 284-288
109 Roberts S A, Findlay R, Lang S D. Investigation of an outbreak of multi-drug resistant Acinetobacter baumannii in an intensive care burns unit. J Hosp Infect . 2001; 48 228-232
110 Levidiotou S, Galanakis E, Vrioni G, Papamichael D, Nakos G, Stefanou D. A multi-resistant Acinetobacter baumannii outbreak in a general intensive care unit. In Vivo . 2002; 16 117-122
111 Webster C A, Crowe M, Humphreys H, Towner K J. 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; 17 171-176
112 Riley T V, Webb S A, Cadwallader H, Briggs B D, Christiansen L, Bowman R A. Outbreak of gentamicin-resistant Acinetobacter baumanii in an intensive care unit: clinical, epidemiological and microbiological features. Pathology . 1996; 28 359-363
113 Van Dessel H, Kamp-Hopmans T E, Fluit A C. Outbreak of a susceptible strain of Acinetobacter species 13 (sensu Tjernberg and Ursing) in an adult neurosurgical intensive care unit. J Hosp Infect . 2002; 51 89-95
114 Ahmed J, Brutus A, D'Amato R F, Glatt A E. Acinetobacter calcoaceticus anitratus outbreak in the intensive care unit traced to a peak flow meter. Am J Infect Control . 1994; 22 319-321
115 Ritter E, Thurm V, Becker-Boost E, Thomas P, Finger H, Wirsing von Konig H C. [Epidemic occurrences of multiresistant Acinetobacter baumannii strains in a neonatal intensive care unit]. Zentralbl Hyg Umweltmed . 1993; 193 461-470
116 Trilla A. Epidemiology of nosocomial infections in adult intensive care units. Intensive Care Med . 1994; 20(suppl 3) S1-S4
117 Cox T R, Roland W E, Dolan M E. Ventilator-related Acinetobacter outbreak in an intensive care unit. Mil Med . 1998; 163 389-391
118 Dealler S. Nosocomial outbreak of multi-resistant Acinetobacter sp. on an intensive care unit: possible association with ventilation equipment. J Hosp Infect . 1998; 38 147-148
119 Ling M L, Ang A, Wee M, Wang G C. A nosocomial outbreak of multiresistant Acinetobacter baumannii originating from an intensive care unit. Infect Control Hosp Epidemiol . 2001; 22 48-49
120 Van Der Zwet C W, Parlevliet G A, Savelkoul P H. Outbreak of Bacillus cereus infections in a neonatal intensive care unit traced to balloons used in manual ventilation. J Clin Microbiol . 2000; 38 4131-4136
121 Nosocomial Burkholderia cepacia infection and colonization associated with intrinsically contaminated mouthwash-Arizona, 1998. Morb Mortal Wkly Rep . 1998; 47 926-928
122 Centers for Disease Control and Prevention. Nosocomial Burkholderia cepacia infection and colonization associated with intrinsically contaminated mouthwash-Arizona, 1998. JAMA . 1999; 281 318
123 Gravel D, Sample M L, Ramotar K, Toye B, Oxley C, Garber G. Outbreak of Burkholderia cepacia in the adult intensive care unit traced to contaminated indigo-carmine dye. Infect Control Hosp Epidemiol . 2002; 23 103-106
124 Raman T S, Jayaprakash D G, Singh D, Krishnamurthy L, Menon P K. Citrobacter septicemia in neonates. Indian Pediatr . 1993; 30 516-520
125 Thurm V, Gericke B. Identification of infant food as a vehicle in a nosocomial outbreak of Citrobacter freundii: epidemiological subtyping by allozyme, whole-cell protein and antibiotic resistance. J Appl Bacteriol . 1994; 76 553-558
126 Welbel S F, McNeil M M, Kuykendall R J. Candida parapsilosis bloodstream infections in neonatal intensive care unit patients: epidemiologic and laboratory confirmation of a common source outbreak. Pediatr Infect Dis J . 1996; 15 998-1002
127 Finkelstein R, Reinhertz G, Hashman N, Merzbach D. Outbreak of Candida tropicalis fungemia in a neonatal intensive care unit. Infect Control Hosp Epidemiol . 1993; 14 587-590
128 Huang Y C, Lin T Y, Peng H L, Wu J H, Chang H Y, Leu H S. Outbreak of Candida albicans fungaemia in a neonatal intensive care unit. Scand J Infect Dis . 1998; 30 137-142
129 Boccia S, Posteraro B, La Sorda M. Genotypic analysis by 27A DNA fingerprinting of Candida albicans strains isolated during an outbreak in a neonatal intensive care unit. Infect Control Hosp Epidemiol . 2002; 23 281-284
130 Betremieux P, Chevrier S, Quindos G, Sullivan D, Polonelli L, Guiguen C. Use of DNA fingerprinting and biotyping methods to study a Candida albicans outbreak in a neonatal intensive care unit. Pediatr Infect Dis J . 1994; 13 899-905
131 Damjanovic V, Connolly C M, van Saene K H. Selective decontamination with nystatin for control of a Candida outbreak in a neonatal intensive care unit. J Hosp Infect . 1993; 24 245-259
132 Morooka T, Umeda A, Fujita M. Epidemiologic application of pulsed-field gel electrophoresis to an outbreak of Campylobacter fetus meningitis in a neonatal intensive care unit. Scand J Infect Dis . 1996; 28 269-270
133 Alfa M J, Robson D, Davi M, Bernard K, Van Caeseele P, Harding G K. An outbreak of necrotizing enterocolitis associated with a novel Clostridium species in a neonatal intensive care unit. Clin Infect Dis . 2002; 35(suppl 1) S101-S105
134 Camargo L F, Strabelli T M, Ribeiro F G. Epidemiologic investigation of an outbreak of coagulase-negative staphylococcus primary bacteremia in a newborn intensive care unit. Infect Control Hosp Epidemiol . 1995; 16 595-596
135 Enterobacter sakazakii infections associated with the use of powdered infant formula-Tennessee, 2001. Morb Mortal Wkly Rep . 2002; 51 297-300
136 Archibald L K, Ramos M, Arduino M J. Enterobacter cloacae and Pseudomonas aeruginosa polymicrobial bloodstream infections traced to extrinsic contamination of a dextrose multidose vial. J Pediatr . 1998; 133 640-644
137 Yu W L, Cheng H S, Lin H C, Peng C T, Tsai C H. Outbreak investigation of nosocomial Enterobacter cloacae bacteraemia in a neonatal intensive care unit. Scand J Infect Dis . 2000; 32 293-298
138 Verweij P E, Van Belkum A, Melchers W J, Voss A, Hoogkamp-Korstanje J A, Meis J F. Interrepeat fingerprinting of third-generation cephalosporin-resistant Enterobacter cloacae isolated during an outbreak in a neonatal intensive care unit. Infect Control Hosp Epidemiol . 1995; 16 25-29
139 Peters S M, Bryan J, Cole M F. Enterobacterial repetitive intergenic consensus polymerase chain reaction typing of isolates of Enterobacter cloacae from an outbreak of infection in a neonatal intensive care unit. Am J Infect Control . 2000; 28 123-129
140 van Nierop H W, Duse A G, Stewart R G, Bilgeri Y R, Koornhof H J. Molecular epidemiology of an outbreak of Enterobacter cloacae in the neonatal intensive care unit of a provincial hospital in Gauteng, South Africa. J Clin Microbiol . 1998; 36 3085-3087
141 Neuwirth C, Siebor E, Lopez J, Pechinot A, Kazmierczak A. Outbreak of TEM-24-producing Enterobacter aerogenes in an intensive care unit and dissemination of the extended-spectrum beta-lactamase to other members of the family Enterobacteriaceae. J Clin Microbiol . 1996; 34 76-79
142 Arpin C, Coze C, Rogues A M, Gachie J P, Bebear C, Quentin C. Epidemiological study of an outbreak due to multidrug-resistant Enterobacter aerogenes in a medical intensive care unit. J Clin Microbiol . 1996; 34 2163-2169
143 Grattard F, Pozzetto B, Berthelot P. Arbitrarily primed PCR, ribotyping, and plasmid pattern analysis applied to investigation of a nosocomial outbreak due to Enterobacter cloacae in a neonatal intensive care unit. J Clin Microbiol . 1994; 32 596-602
144 Jukka C M, Neal T J, Corkill J E. An outbreak of multiply resistant Enterobacter cloacae in a neonatal intensive care unit. J Hosp Infect . 2001; 48 155-156
145 Herruzo-Cabrera R, Garcia-Caballero J, Martin-Moreno J M, Graciani-Perez-Regadera M A, Perez-Rodriguez J. Clinical assay of N-duopropenide alcohol solution on hand application in newborn and pediatric intensive care units: control of an outbreak of multiresistant Klebsiella pneumoniae in a newborn intensive care unit with this measure. Am J Infect Control . 2001; 29 162-167
146 Donkers L E, van Furth M A, van der Zwet C W, Fetter W P, Roord J J, Vandenbroucke-Grauls C M. [Enterobacter cloacae epidemic on a neonatal intensive care unit due to the use of contaminated thermometers]. Ned Tijdschr Geneeskd . 2001; 145 643-647
147 Dorsey G, Borneo H T, Sun S J. A heterogeneous outbreak of Enterobacter cloacae and Serratia marcescens infections in a surgical intensive care unit. Infect Control Hosp Epidemiol . 2000; 21 465-469
148 Loiwal V, Kumar A, Gupta P, Gomber S, Ramachandran V G. Enterobacter aerogenes outbreak in a neonatal intensive care unit. Pediatr Int . 1999; 41 157-161
149 Lucet J C, Chevret S, Decre D. Outbreak of multiply resistant Enterobacteriaceae in an intensive care unit: epidemiology and risk factors for acquisition. Clin Infect Dis . 1996; 22 430-436
150 Acolet D, Ahmet Z, Houang E, Hurley R, Kaufmann M E. Enterobacter cloacae in a neonatal intensive care unit: account of an outbreak and its relationship to use of third generation cephalosporins. J Hosp Infect . 1994; 28 273-286
151 Hoque S N, Graham J, Kaufmann M E, Tabaqchali S. Chryseobacterium (Flavobacterium) meningosepticum outbreak associated with colonization of water taps in a neonatal intensive care unit. J Hosp Infect . 2001; 47 188-192
152 Campbell J R, Arango C A, Garcia-Prats J A, Baker C J. An outbreak of M serotype 1 group A streptococcus in a neonatal intensive care unit. J Pediatr . 1996; 129 396-402
153 Kalenic S, Jandrlic M, Vegar V, Zuech N, Sekulic A, Mlinaric-Missoni E. Hansenula anomala outbreak at a surgical intensive care unit: a search for risk factors. Eur J Epidemiol . 2001; 17 491-496
154 Hanna J N, Loewenthal M R, Negel P, Wenck D J. An outbreak of hepatitis A in an intensive care unit. Anaesth Intensive Care . 1996; 24 440-444
155 Watson J C, Fleming D W, Borella A J, Olcott E S, Conrad R E, Baron R C. Vertical transmission of hepatitis A resulting in an outbreak in a neonatal intensive care unit. J Infect Dis . 1993; 167 567-571
156 Cunney R J, Bialachowski A, Thornley D, Smaill F M, Pennie R A. An outbreak of influenza A in a neonatal intensive care unit. Infect Control Hosp Epidemiol . 2000; 21 449-454
157 Munoz F M, Campbell J R, Atmar R L. Influenza A virus outbreak in a neonatal intensive care unit. Pediatr Infect Dis J . 1999; 18 811-815
158 Jeong S H, Kim W M, Chang C L. Neonatal intensive care unit outbreak caused by a strain of Klebsiella oxytoca resistant to aztreonam due to overproduction of chromosomal beta-lactamase. J Hosp Infect . 2001; 48 281-288
159 Asensio A, Oliver A, Gonzalez-Diego P. Outbreak of a multiresistant Klebsiella pneumoniae strain in an intensive care unit: antibiotic use as risk factor for colonization and infection. Clin Infect Dis . 2000; 30 55-60
160 van der Zwet C W, Parlevliet G A, Savelkoul P H. Nosocomial outbreak of gentamicin-resistant Klebsiella pneumoniae in a neonatal intensive care unit controlled by a change in antibiotic policy. J Hosp Infect . 1999; 42 295-302
161 Flidel-Rimon O, Leibovitz E, Juster-Reicher A. An outbreak of antibiotic multiresistant Klebsiella at the Neonatal Intensive Care Unit, Kaplan Hospital, Rehovot, Israel, November 1991 to April 1992. Am J Perinatol . 1996; 13 99-102
162 Rebuck J A, Olsen K M, Fey P D, Langnas A N, Rupp M E. Characterization of an outbreak due to extended-spectrum beta-lactamase-producing Klebsiella pneumoniae in a pediatric intensive care unit transplant population. Clin Infect Dis . 2000; 31 1368-1372
163 Martinez-Aguilar G, Alpuche-Aranda C M, Anaya C. Outbreak of nosocomial sepsis and pneumonia in a newborn intensive care unit by multiresistant extended-spectrum beta-lactamase-producing Klebsiella pneumoniae: high impact on mortality. Infect Control Hosp Epidemiol . 2001; 22 725-728
164 Otman J, Cavassin E D, Perugini M E, Vidotto M C. An outbreak of extended-spectrum beta-lactamase-producing Klebsiella species in a neonatal intensive care unit in Brazil. Infect Control Hosp Epidemiol . 2002; 23 8-9
165 Archer-Dubon C, Icaza-Chivez M E, Orozco-Topete R, Reyes E, Baez-Martinez R, Ponce de Leon S. An epidemic outbreak of Malassezia folliculitis in three adult patients in an intensive care unit: a previously unrecognized nosocomial infection. Int J Dermatol . 1999; 38 453-456
166 Chang H J, Miller H L, Watkins N. An epidemic of Malassezia pachydermatis in an intensive care nursery associated with colonization of health care workers' pet dogs. N Engl J Med . 1998; 338 706-711
167 Welbel S F, McNeil M M, Pramanik A. Nosocomial Malassezia pachydermatis bloodstream infections in a neonatal intensive care unit. Pediatr Infect Dis J . 1994; 13 104-108
168 Nakano M, Miyazawa H, Kawano Y. An outbreak of neonatal toxic shock syndrome-like exanthematous disease (NTED) caused by methicillin-resistant Staphylococcus aureus (MRSA) in a neonatal intensive care unit. Microbiol Immunol . 2002; 46 277-284
169 Jumaa P, Chattopadhyay B. Outbreak of gentamicin, ciprofloxacin-resistant Pseudomonas aeruginosa in an intensive care unit, traced to contaminated quivers. J Hosp Infect . 1994; 28 209-218
170 Becks V E, Lorenzoni N M. Pseudomonas aeruginosa outbreak in a neonatal intensive care unit: a possible link to contaminated hand lotion. Am J Infect Control . 1995; 23 396-398
171 Garland S M, Mackay S, Tabrizi S, Jacobs S. Pseudomonas aeruginosa outbreak associated with a contaminated blood-gas analyser in a neonatal intensive care unit. J Hosp Infect . 1996; 33 145-151
172 Bert F, Maubec E, Bruneau B, Berry P, Lambert-Zechovsky N. Multi-resistant Pseudomonas aeruginosa outbreak associated with contaminated tap water in a neurosurgery intensive care unit. J Hosp Infect . 1998; 39 53-62
173 Trick W E, Kioski C M, Howard K M. Outbreak of Pseudomonas aeruginosa ventriculitis among patients in a neurosurgical intensive care unit. Infect Control Hosp Epidemiol . 2000; 21 204-208
174 Kerr J R, Moore J E, Curran M D. Investigation of a nosocomial outbreak of Pseudomonas aeruginosa pneumonia in an intensive care unit by random amplification of polymorphic DNA assay. J Hosp Infect . 1995; 30 125-131
175 Talon D, Capellier G, Boillot A, Michel-Briand Y. Use of pulsed-field gel electrophoresis as an epidemiologic tool during an outbreak of Pseudomonas aeruginosa lung infections in an intensive care unit. Intensive Care Med . 1995; 21 996-1002
176 Sader H S, Pignatari A C, Leme I L. Epidemiologic typing of multiply drug-resistant Pseudomonas aeruginosa isolated from an outbreak in an intensive care unit. Diagn Microbiol Infect Dis . 1993; 17 13-18
177 Tassios P T, Gennimata V, Spaliara-Kalogeropoulou L. Multiresistant Pseudomonas aeruginosa serogroup O:11 outbreak in an intensive care unit. Clin Microbiol Infect . 1997; 3 621-628
178 Bertrand X, Bailly P, Blasco G, Balvay P, Boillot A, Talon D. Large outbreak in a surgical intensive care unit of colonization or infection with Pseudomonas aeruginosa that overexpressed an active efflux pump. Clin Infect Dis . 2000; 31 E9-E14
179 Moolenaar R L, Crutcher J M, San Joaquin H V. A prolonged outbreak of Pseudomonas aeruginosa in a neonatal intensive care unit: did staff fingernails play a role in disease transmission?. Infect Control Hosp Epidemiol . 2000; 21 80-85
180 Orrett F A. Fatal multi-resistant Pseudomonas aeruginosa septicemia outbreak in a neonatal intensive care unit in Trinidad. Ethiop Med J . 2000; 38 85-91
181 Miranda G, Leanos B, Marquez L. Molecular epidemiology of a multiresistant Pseudomonas aeruginosa outbreak in a paediatric intensive care unit. Scand J Infect Dis . 2001; 33 738-743
182 Newman M J. Multiple-resistant Salmonella group G outbreak in a neonatal intensive care unit. West Afr J Med . 1996; 15 165-169
183 Mahajan R, Mathur M, Kumar A, Gupta P, Faridi M M, Talwar V. Nosocomial outbreak of Salmonella typhimurium infection in a nursery intensive care unit (NICU) and paediatric ward. J Commun Dis . 1995; 27 10-14
184 Umasankar S, Mridha E U, Hannan M M, Fry C M, Azadian B S. An outbreak of Salmonella enteritidis in a maternity and neonatal intensive care unit. J Hosp Infect . 1996; 34 117-122
185 Ostrowsky B E, Whitener C, Bredenberg H K, et al. Serratia marcescens bacteremia traced to an infused narcotic. N Engl J Med . 2002; 346 1529-1537
186 Pagani L, Luzzaro F, Ronza P. Outbreak of extended-spectrum beta-lactamase-producing Serratia marcescens in an intensive care unit. FEMS Immunol Med Microbiol . 1994; 10 39-46
187 Miranda G, Kelly C, Solorzano F, Leanos B, Coria R, Patterson J E. Use of pulsed-field gel electrophoresis typing to study an outbreak of infection due to Serratia marcescens in a neonatal intensive care unit. J Clin Microbiol . 1996; 34 3138-3141
188 Miranda-Novales M G, Gordillo-Perez M G, Solorzano-Santos F, Leanos-Miranda B, Villasis-Keever M A, Villegas-Silva R. [Case-control study of an outbreak of Smarcescens in a neonatal intensive care unit]. Rev Invest Clin . 1998; 50 13-18
189 Jang T N, Fung C P, Yang T L, Shen S H, Huang C S, Lee S H. Use of pulsed-field gel electrophoresis to investigate an outbreak of Serratia marcescens infection in a neonatal intensive care unit. J Hosp Infect . 2001; 48 13-19
190 Prasad G A, Jones P G, Michaels J, Garland J S, Shivpuri C R. Outbreak of Serratia marcescens infection in a neonatal intensive care unit. Infect Control Hosp Epidemiol . 2001; 22 303-305
191 Villari P, Crispino M, Salvadori A, Scarcella A. Molecular epidemiology of an outbreak of Serratia marcescens in a neonatal intensive care unit. Infect Control Hosp Epidemiol . 2001; 22 630-634
192 Falk P S, Winnike J, Woodmansee C, Desai M, Mayhall C G. Outbreak of vancomycin-resistant enterococci in a burn unit. Infect Control Hosp Epidemiol . 2000; 21 575-582
193 Hanna H, Umphrey J, Tarrand J, Mendoza M, Raad I. Management of an outbreak of vancomycin-resistant enterococci in the medical intensive care unit of a cancer center. Infect Control Hosp Epidemiol . 2001; 22 217-219
194 Lee H K, Lee W G, Cho S R. Clinical and molecular biological analysis of a nosocomial outbreak of vancomycin-resistant enterococci in a neonatal intensive care unit. Acta Paediatr . 1999; 88 651-654