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Year : 2010  |  Volume : 28  |  Issue : 1  |  Page : 5-10

Clinical microbiology in the intensive care unit: Strategic and operational characteristics

1 Department of Microbiology, West Suffolk Hospital NHS Trust , Bury St. Edmund, United Kingdom
2 Department of Anaesthesia and Intensive Care, North Middlesex University Hospital , London, United Kingdom

Date of Submission11-Aug-2009
Date of Acceptance28-Sep-2009
Date of Web Publication6-Jan-2010

Correspondence Address:
S Bhattacharya
Department of Microbiology, West Suffolk Hospital NHS Trust , Bury St. Edmund
United Kingdom
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0255-0857.58720

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 ~ Abstract 

Infection is a major cause of morbidity and mortality among patients admitted in intensive care units (ICUs). The application of the principles and the practice of Clinical Microbiology for ICU patients can significantly improve clinical outcome. The present article is aimed at summarising the strategic and operational characteristics of this unique field where medical microbiology attempts to venture into the domain of direct clinical care of critically ill patients. The close and strategic partnership between clinical microbiologists and intensive care specialists, which is essential for this model of patient care have been emphasized. The article includes discussions on a variety of common clinical-microbiological problems faced in the ICUs such as ventilator-associated pneumonia, blood stream infections, skin and soft tissue infection, UTI, infection control, besides antibiotic management.

Keywords: Clinical microbiology, intensive care unit, antibiotics

How to cite this article:
Bhattacharya S, Mondal A S. Clinical microbiology in the intensive care unit: Strategic and operational characteristics. Indian J Med Microbiol 2010;28:5-10

How to cite this URL:
Bhattacharya S, Mondal A S. Clinical microbiology in the intensive care unit: Strategic and operational characteristics. Indian J Med Microbiol [serial online] 2010 [cited 2020 Jul 8];28:5-10. Available from:

 ~ Introduction Top

Infection is a major factor determining clinical outcome among patients requiring intensive care unit (ICU) support. [1] The causes of infection within ICU are multi-factorial, and consequences depend on source involved, organisms associated, underlying morbidity, timeliness and appropriateness of the treatment/ interventions received. Apart from the clinical and human consequences, the health economic and infection control implications of infection within ICU are huge. [2] This article is an attempt to summarise infection management strategies within ICUs using clinical microbiology-intensive care partnership as a standard model.

Clinical profile of patients requiring intensive care support

Any clinical event, which compromises the airway, breathing, circulation (ABC) of a patient or breaches significantly the integrity and functioning of tissues and organs (post surgery, post trauma) may result in the requirement of ICU or high dependency unit (HDU) support. These incidents can be either unexpected clinical emergencies (cerebro-vascular accidents, acute myocardial infarction, severe sepsis, fulminant hepatitis, acute pancreatitis, road traffic accidents, burns and other forms of physical trauma, intoxication), or may follow planned elective procedures (neuro-surgery, coronary artery bypass grafting, intra-abdominal surgeries). The care provided to patients within the ICU setting may include basic life support (airway, breathing, fluid-electrolyte balance, nutrition), routine or specialised organ support (artificial ventilation, intra-cardiac balloon pump, haemo-filtration, extra-corporeal membrane oxygenation-ECMO, molecular adsorbent recirculation system-MARS) besides directed therapy against infection or inflammation. Consequently, the ICU support offered in hospitals has diversified into sub-specialties such as general ICU (for patients coming with sepsis, pneumonia, pancreatitis, post trauma, post abdominal surgery), cardiothoracic ICU (post CABG, heart failure), neuro-ICU (post neurosurgery, head injury), and neonatal/paediatric ICU (for pre-term and low birth weight babies, and babies in need of specialised care for medical or surgical reasons). This life supporting system involves a continuous monitoring of the vital parameters (pulse rate, respiratory rate, temperature, blood pressure) and organ function (oxygen saturation, arterial blood gas analysis, haematological and biochemical monitoring of liver/ renal function, level of consciousness and routine physical examination). Modern intensive care is a multi-disciplinary effort of a team lead by the intensivist, but supported as and when required by associated medical/surgical specialities.

Infections among patients in the intensive care unit

Infection among ICU patients might be community acquired (viral encephalitis, bacterial meningitis, pneumonia, endocarditis, intra-visceral abscesses, urinary tract infections-UTIs) or hospital and health care associated infections (surgical site infections- SSIs, hospital acquired pneumonia-HAP, catheter related blood stream infections - CR-BSI, catheter associated UTI). [1] The consequence and complications of infection might have variable clinical (sepsis, organ failure, death), health economic (bed utilisation, hospital stay, cost of care, antibiotic utilisation), infection control impact (spread of infection to patient/ staff/ visitor). A sustained partnership between the intensivist and the clinical microbiologist is essential for improving clinical outcomes and optimising resource utilisation.

Typical microbiological challenges within ICUs

  1. Limited time and narrow window of opportunity to diagnose, treat or intervene because of critical illness. The cost of delay or failure is often death or grievous organ damage to the patient
  2. Single or multiple organ failure in the patient leading to inadequate tissue penetration of antimicrobial agents or suboptimal drug metabolism and elimination (altered pharmaco-kinetics and pharmacodynamics)
  3. High antimicrobial usage leading to increased cost, anti-microbial resistance, CDAD (Clostridium difficile associated diarrhoea)
  4. Lack of side room or isolation facilities leading to greater infection control risks

 ~ Common Health Care Associated Infections in intensive care unit Patients Top

Ventilator associated pneumonia

Patients requiring artificial mechanical ventilation are susceptible to infection due to micro-aspiration of oropharyngeal or gastric secretions leading to lower respiratory tract infection. Common pathogens include organisms present in patient's own upper respiratory tract (Staphylococcus spp., Streptococci., Haemophilus influenzae, oral anaerobes) as well as those present in the hospital environment (mainly aerobic Gram negative bacilli such as Eschericia coli, Klebsiella spp., Pseudomonas spp., Acinetobacter spp.). The patient may manifest with local (coarse crackles on auscultation, increased oxygen requirement manifested as increase in FiO 2 , new chest X ray infiltration) usually along with systemic manifestations of infection. Specific identification of causative organism is often difficult because of the paucity of good quality samples, which often require invasive sampling (bronco- alveolar lavage, protected bronchial brush or non-directed bronchial lavage). The presence of bacteria in the sample, do not necessarily signify infection (colonisation of upper respiratory tract with Gram-negative bacilli or Candida is common in hospitalised/antibiotic treated patients). Hence in most cases antibiotic choice is empirical and based on circumstantial, epidemiological and clinical evidence. Therapy generally involves giving broad-spectrum antibiotics to cover putative Gram positive and Gram-negative pathogens (Piperacillin-Tazobactum, Carbapenems such as Imipenem or Meropenem). In specific situations, depending on positive microbiology specific directed therapy may have to be added (such as Vancomycin or Linezolid for MRSA; Fluconazole, Caspofungin or Amphotericin B for Candida albicans or other Candida species). The duration of therapy depends on clinical response, pathogens involved, underlying risk factors and co-morbidities. In recent years VAP care bundles consisting of elevation of the head of the bed to 30-45 degrees, daily 'sedation vacation' and daily assessment of readiness to extubate, peptic ulcer disease prophylaxis, and deep venous thrombosis prophylaxis have been shown to improve outcome. [3],[4]

Skin and soft tissue infection

This may either take the form of surgical site infection (SSI), vascular catheter induced phlebitis (VIP) with or without adjoining infection of skin and soft tissues, and pressures sores (decubitus/pressure ulcers and stress ulcers). While appropriate peri-operative antibiotics have a role in prevention of SSI it is no substitute for good surgical techniques. Prevention is the mainstay in the management of VIP and pressure ulcers, because once developed the treatment could not only be difficult (e.g. pressure sores), and prolonged (leading to increased hospital stay and its consequences) but also life threatening through the development of sepsis. The evidence regarding the efficacy of antibiotic prophylaxis in preventing post-operative infections is highly variable. Although there are clearly areas where the benefit of peri-operative antibiotics is fairly well established, [5],[6],[7] there are areas where there either no evidence that prophylaxis has any effect, [8] or the evidence on either side of the argument does not exist because of lack of adequate studies. [9] It is important that evidence based recommendations for surgical prophylaxis is adhered to not only in the choice and dose of agent but also for the duration. Various evidence based guidelines from Cochrane and other sources (e.g. Scottish Intercollegiate Guideline Network-SIGN) [10] are available. Prolonged antibiotic use in the peri-operative period not only lack justification but also contribute to subsequent problems (selection of resistant strains, C. difficile associated diarrhoea) besides unnecessarily increasing cost of care. For the prevention of VIP and associated SSTI, adherence to the three-day rule is important so that the need for intravenous access is seriously reviewed on a daily basis, and no peripheral venous catheters are left for more than 72 hours. [11],[12] This requires documentation (with time, date, site, name of the person responsible for insertion and assessment) so that regular audits could be conducted as and when required. [13] Although the pathogenesis of pressure ulcers appears to be multi-factorial, [14] scrupulous attention to the integrity of skin is paramount in the prevention of decubitus ulcers in debilitated and critically ill patients because once established these lesions especially if they involve deeper tissues are notoriously difficult to manage and may cost not only the well being and potentially the life of the patient but also the reputation of institution and health care workers (physicians and nurses) responsible for the patient care. Good hygiene, adequate nutrition, patient mobility, special bed mattress, and adequate nurse patient ratio is critical if this condition is to be avoided. [15],[16],[17],[18],[19]

Blood stream infections (BSIs) including catheter related

This constitutes an important cause of morbidity and mortality among patients in critical care settings and other clinical areas. BSIs that accompany primary diseases such as infective endocarditis, community acquired pneumonia, uro-sepsis and meningitis are not being discussed here. This section is only dealing with BSIs that may result from health care interventions such as a vascular catheter insertion, secondary bacteremia following urinary catheter related sepsis, infection of surgical sites or infection arising out of hospital acquired or ventilator related pneumonia. Vascular access devices are inserted in critically ill patients for the maintenance of fluid-electrolyte balance, administration of therapeutic agents (vasoactive drugs, antibiotics, etc.), maintain nutritional requirements (TPN- total parenteral nutrition), monitoring vital parameters (e.g. central venous pressure, arterial pressure), providing vital organ support (e.g. haemo-filtration), and doing essential investigations (blood gas monitoring, besides routine haematological and biochemical tests). Again, the only way to avoid infections from these essential interventions include strict and meticulous attention to asepsis during insertion of vascular access devices, regular mapping and review of each vascular channel so that they are kept only as long as essential. There is evidence that the use of chlorhexidine-based preparations and insertion of central line through the sub-clavian access (in contrast to internal jugular or femoral access) reduce infection rates. [20] Most patients with BSIs are likely to manifest clinically with systemic signs of infection (fever, leucocytosis, raised inflammatory markers) and blood cultures both peripheral and through the vascular access device need to be taken within 15 minutes of each other detect CR-BSI. Empirical therapy should constitute glycopeptide antibiotics such as Vancomycin to cover common Gram-positive pathogens (Methicillin sensitive and resistant Staphylococcus aureus and S. epidermidis) but in most cases CR-BSI removal of the vascular access device remains the mainstay to prevent future episodes or complications (e.g. endocarditis). [21]

Urinary tract infection

Urinary catheters are used in the ICU setting to monitor urine output, relieve retention and facilitate nursing care. However, each episode of urinary catheter insertion constitutes an infection risk and the catheter need should be reviewed on a day-to-day basis and should be present only as long as clinically indicated. Most catheters get colonised by bacteria within a few days, therefore the presence of bacteria in catheterised specimen of urine (CSU) is common and does not necessarily warrant antibiotic therapy. [22] Therefore, the decision to initiate antibiotic therapy has to be individualised and systemic and local signs of infection are more important than CSU microbiology and cytology. During the process of change of catheter a single shot of gentamicin (2 mg/kg body weight iv) or other appropriate antibiotics with a good urinary excretion can help prevent sepsis during the catheter change in sensitive strains. Finally, flushing of blocked catheters might actually be harmful because of chance of developing ascending infection of the upper urinary tract (e.g. pyelonephritis). [23]

 ~ Key Clinical Microbiology Strategies for Infection Management within Intensive Care Units Top

Regular ICU rounds by Clinical Microbiologists with bed-side discussion with Intensivists regarding infection management

In many institutions (for example in the UK) where clinical microbiology as opposed to laboratory centred approach is the mode of practice ICU rounds by microbiologists on a regular basis is common. [24] The objectives of this bedside round are multi-focal and have been elaborated in the subsequent points. This round is crucial for efficient management of infection in critical care and is based on partnership and mutual understanding of microbiological and intensive care perspectives.

Prompt communication of urgent microbiology/virology results

Delay in communication of clinically significant microbiology results and consequently the delay in initiating the appropriate anti-infective therapy or intervention can adversely affect the clinical outcome of a patient in ICU. Clinical microbiology ward round achieves this objective through early communication of even preliminary results so that therapy can be initiated at the earliest opportunity.

Assessment of infection

This constitutes the central objective of the clinical microbiology round in ICU so that diagnostic, therapeutic and infection control interventions can be initiated at the earliest. Assessment of infection is and has to be a broad based approach relying on an entire gamut of historical, epidemiological, clinical, diagnostic parameters (physical examination, haematological, biochemical, radiological) and not just based on microbiology results (positive or negative).

Change, stoppage, optimisation and augmentation of antimicrobial therapy

This constitutes one of the most important interventions offered by clinical microbiologists in ICU, and a consensual approach in consultation with the intensivists is taken with regard to change of any anti-infective therapy. What is required to make this intervention from microbiologists effective is not just the knowledge of resistance mechanisms and antibiotic spectrum but also a detailed understanding of acute physiology, pharmacokinetic-pharmacodynamic effects, and the ability to see the patient as a whole and not just from a microbiological point of view. The [Table 1] provides a general guide for selection of anti-infective therapy in various important infective syndromes seen in ICUs.

Infection prevention and control

In the ICU setting achieving the objective of preventing the spread of infection from patient/staff/visitor to patient/ staff/visitor can be challenging because of the need to balance the lack resource and information availability with the clinical need of the patient. Universal precautions and scrupulous attention to the adherence of best practice guidelines is the way to prevent hospital-acquired infections. The risk of transmission of infection is real and several interventions such as endo-tracheal intubation (e.g. swine flu, tuberculosis, meningococcal meningitis), vascular catheter insertion (e.g. risk of sharps injury or splash and consequent risk of blood borne viruses) can affect the health care workers (HCWs). Transmission of multi-resistant pathogens (MRSA, [25],[26] ESBL, [27],[28] multi-resistant Acinetobacter baumannii[29],[30] ) has been reported in ICU besides posing significant infection control problems with regard to varicella [31],[32] and tuberculosis [33],[34],[35] (especially in neonatal intensive care units).

Microbiology result interpretation and feedback to intensive care unit team regarding antimicrobial resistance, audit and policy implementation

With the training and knowledge base, microbiologists during intensive care rounds are in a unique position to directly interact with clinicians or patients to explain clinical significance of test results (e.g. infection versus colonisation, predictive value of test results, significant titres of serology tests, meaning of a PCR result). This may translate not only to better understanding of the significance of microbiology test results but more judicious use of diagnostic tests and anti-infective therapy.

Rational utilisation of diagnostic, therapeutic and infection prevention/control resources

One of the challenges in clinical microbiology is to optimise and rationalise the use of sparse resources so as to deliver the greatest good for the maximum number of patients keeping in mind the limitations of resource availability (diagnostic test, therapeutic option, infection control facilities). Each ICU is different from the other in terms of the patient/staff profile and resource availability so development of local guidelines in consultation with all relevant departments is essential to optimise patient care.

 ~ Conclusions Top

Microbiology has already made a transition from pathological subspecialty to an essential clinical support service. It is important that we accelerate this transition of microbiology to the frontline of direct patient care, viz., the ICU. Many lives are either saved or lost in the ICU setting of every major hospital. Infection is a major contributor to adverse patient outcome. Close partnership between microbiologists and intensive care physicians can save many more lives. "Care bundles," used in ICU setting either for management of sepsis or management of patients requiring ventilation, are setting the standards of care. [36],[37],[38] There is no reason why a number of "infection service bundles" [39] comprising of appropriate uses of diagnostic-therapeutic-infection control resources, which are monitored and tailored by clinical microbiologists and supported by intensivists cannot become an integral part of ICU package.

 ~ References Top

1.Vincent JL, Bihari DJ, Suter PM, Bruining HA, White J, Nicolas-Chanoin MH, et al. 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;274:639-44.  Back to cited text no. 1      
2.Chen YY, Wang FD, Liu CY, Chou P. Incidence rate and variable cost of nosocomial infections in different types of intensive care units. Infect Control Hosp Epidemiol 2009;30:39-46.  Back to cited text no. 2      
3.Blamoun J, Alfakir M, Rella ME, Wojcik JM, Solis RA, Anees Khan M, et al. Efficacy of an expanded ventilator bundle for the reduction of ventilator-associated pneumonia in the medical intensive care unit. Am J Infect Control 2009;37:172-5.  Back to cited text no. 3      
4.Wip C, Napolitano L. Bundles to prevent ventilator-associated pneumonia: How valuable are they? Curr Opin Infect Dis 2009;22:159-66.  Back to cited text no. 4      
5.Gillespie WJ, Walenkamp G. Antibiotic prophylaxis for surgery for proximal femoral and other closed long bone fractures. Cochrane Database Syst Rev 2001;1:CD000244.  Back to cited text no. 5      
6.Andersen BR, Kallehave FL, Andersen HK. Antibiotics versus placebo for prevention of postoperative infection after appendicectomy. Cochrane Database Syst Rev 2005;3:CD001439.  Back to cited text no. 6      
7.Cunningham M, Bunn F, Handscomb K. Prophylactic antibiotics to prevent surgical site infection after breast cancer surgery. Cochrane Database Syst Rev 2006;2:CD005360.  Back to cited text no. 7      
8.Verschuur HP, de Wever WW, van Benthem PP. Antibiotic prophylaxis in clean and clean-contaminated ear surgery. Cochrane Database Syst Rev 2004;3:CD003996.  Back to cited text no. 8      
9.Liabsuetrakul T, Choobun T, Peeyananjarassri K, Islam M. Antibiotic prophylaxis for operative vaginal delivery. Cochrane Database Syst Rev 2004;3:CD004455.  Back to cited text no. 9      
10.Scottish Intercollegiate Guideline Network. Antibiotic prophylaxis in surgery. Available from: Http:// [last accessed on 2009 Aug 9].  Back to cited text no. 10      
11.Abbas SZ, de Vries TK, Shaw S, Abbas SQ. Use and complications of peripheral vascular catheters: A prospective study. Br J Nurs 2007;16:648-52.  Back to cited text no. 11      
12.Goddard L, Clayton S, Peto TE, Bowler IC. The ′just-in-case venflon′: Effect of surveillance and feedback on prevalence of peripherally inserted intravascular devices. J Hosp Infect 2006;64:401-2.  Back to cited text no. 12      
13.Shapey IM, Foster MA, Whitehouse T, Jumaa P, Bion JF. Central venous catheter-related bloodstream infections: Improving post-insertion catheter care. J Hosp Infect 2009;71:117-22.  Back to cited text no. 13      
14.Terekeci H, Kucukardali Y, Top C, Onem Y, Celik S, Oktenli C. Risk assessment study of the pressure ulcers in intensive care unit patients. Eur J Intern Med 2009;20:394-7.  Back to cited text no. 14      
15.Vowden KR, Vowden P. The prevalence, management, equipment provision and outcome for patients with pressure ulceration identified in a wound care survey within one English health care district. J Tissue Viability 2009;18:20-6.  Back to cited text no. 15      
16.Gallagher P, Barry P, Hartigan I, McCluskey P, O′Connor K, O′Connor M. Prevalence of pressure ulcers in three university teaching hospitals in Ireland. J Tissue Viability 2008;17:103-9.   Back to cited text no. 16      
17.Yang KP. Relationships between nurse staffing and patient outcomes. J Nurs Res 2003;11:149-58.  Back to cited text no. 17      
18.Gunningberg L. Risk, prevalence and prevention of pressure ulcers in three Swedish healthcare settings. J Wound Care 2004;13:286-90.  Back to cited text no. 18 Laat EH, Pickkers P, Schoonhoven L, Verbeek AL, Feuth T, van Achterberg T. Guideline implementation results in a decrease of pressure ulcer incidence in critically ill patients. Crit Care Med 2007;35:815-20.  Back to cited text no. 19      
20.Ruschulte H, Franke M, Gastmeier P, Zenz S, Mahr KH, Buchholz S, et al. Prevention of central venous catheter related infections with chlorhexidine gluconate impregnated wound dressings: A randomized controlled trial. Ann Hematol 2009;88:267-72.  Back to cited text no. 20      
21.Mermel LA, Allon M, Bouza E, Craven DE, Flynn P, O′Grady NP, et al. Clinical practice guidelines for the diagnosis and management of intravascular catheter-related infection: 2009 Update by the Infectious Diseases Society of America. Clin Infect Dis 2009;49:1-45.  Back to cited text no. 21      
22.Wiseman O. Management of the long-term urinary catheter in the asymptomatic patient in the Accident and Emergency department. Br J Urol 1997;80:748-51.  Back to cited text no. 22      
23.Nicolle LE. Catheter-related urinary tract infection. Drugs Aging 2005;22:627-39.  Back to cited text no. 23      
24.The Royal College of Pathologist. Specimen job description: Consultant medical microbiologist. April 2005.  Back to cited text no. 24      
25.Khan A, Lampitoc M, Salaripour M, McKernan P, Devlin R, Muller MP. Rapid control of a methicillin resistant Staphylococcus aureus (MRSA) outbreak in a medical surgical intensive care unit (ICU). Can J Infect Control 2009;24:12-6.  Back to cited text no. 25      
26.Bertin ML, Vinski J, Schmitt S, Sabella C, Danziger-Isakov L, McHugh M, et al. Outbreak of methicillin-resistant Staphy lococcus aureus colonization and infection in a neonatal intensive care unit epidemiologically linked to a healthcare worker with chronic otitis. Infect Control Hosp Epidemiol 2006;27:581-5.  Back to cited text no. 26      
27.Carrλr A, Lassel L, Fortineau N, Mansouri M, Anguel N, Richard C, et al. Outbreak of CTX-M-15-Producing Klebsiella pneumoniae in the Intensive Care Unit of a French Hospital. Microb Drug Resist 2009;15:47-54.  Back to cited text no. 27      
28.Laurent C, Rodriguez-Villalobos H, Rost F, Strale H, Vincent JL, Deplano A, et al. Intensive care unit outbreak of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae controlled by cohorting patients and reinforcing infection control measures. Infect Control Hosp Epidemiol 2008;29:517-24.  Back to cited text no. 28      
29.Touati A, Achour W, Cherif A, Hmida HB, Afif FB, Jabnoun S, et al. Outbreak of Acinetobacter baumannii in a neonatal intensive care unit: Antimicrobial susceptibility and genotyping analysis. Ann Epidemiol 2009;19:372-8.  Back to cited text no. 29      
30.Pimentel JD, Low J, Styles K, Harris OC, Hughes A, Athan E. Control of an outbreak of multi-drug-resistant Acinetobacter baumannii in an intensive care unit and a surgical ward. J Hosp Infect 2005;59:249-53.   Back to cited text no. 30      
31.Ng PC, Lyon DJ, Wong MY, Fok TF, Wong W, Cheung KL, et al. Varicella exposure in a neonatal intensive care unit: Emergency management and control measures. J Hosp Infect 1996;32:229-36.  Back to cited text no. 31      
32.Friedman CA, Temple DM, Robbins KK, Rawson JE, Wilson JP, Feldman S. Outbreak and control of varicella in a neonatal intensive care unit. Pediatr Infect Dis J 1994;13:152-4.  Back to cited text no. 32      
33.Isaacs D, Jones CA, Dalton D, Cripps T, Vidler L, Rochefort M, et al. Exposure to open tuberculosis on a neonatal unit. J Paediatr Child Health 2006;42:557-9.  Back to cited text no. 33      
34.Sen M, Gregson D, Lewis J. Neonatal exposure to active pulmonary tuberculosis in a health care professional. CMAJ 2005;172:1453-6.  Back to cited text no. 34      
35.Laartz BW, Narvarte HJ, Holt D, Larkin JA, Pomputius WF 3 rd . Congenital tuberculosis and management of exposures in a neonatal intensive care unit. Infect Control Hosp Epidemiol 2002;23:573-9.  Back to cited text no. 35      
36.Ferrer R, Artigas A, Levy MM, Blanco J, Gonzαlez-Dνaz G, Garnacho-Montero J, et al. Edusepsis Study Group. Improvement in process of care and outcome after a multicenter severe sepsis educational program in Spain. JAMA 2008;299:2294-303.  Back to cited text no. 36      
37.Marwick C, Davey P. Care bundles: The holy grail of infectious risk management in hospital? Curr Opin Infect Dis 2009;22:364-9.  Back to cited text no. 37      
38.Lachman P, Yuen S. Using care bundles to prevent infection in neonatal and paediatric ICUs. Curr Opin Infect Dis 2009;22:224-8.  Back to cited text no. 38      
39.Health Protection Scotland. Infection Control-Bundles. Available from: Http:// CareBundle.aspx [last accessed on 2009 Aug 9].  Back to cited text no. 39      


  [Table 1]


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