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1.  From intermittent antibiotic point prevalence surveys to quality improvement: experience in Scottish hospitals 
Background
In 2008, the Scottish Antimicrobial Prescribing Group (SAPG) was established to coordinate a national antimicrobial stewardship programme. In 2009 SAPG led participation in a European point prevalence survey (PPS) of hospital antibiotic use. We describe how SAPG used this baseline PPS as the foundation for implementation of measures for improvement in antibiotic prescribing.
Methods
In 2009 data for the baseline PPS were collected in accordance with the European Surveillance of Antimicrobial Consumption [ESAC] protocol. This informed the development of two quality prescribing indicators: compliance with antibiotic policy in acute admission units and duration of surgical prophylaxis. From December 2009 clinicians collected these data on a monthly basis. The prescribing indicators were reviewed and further modified in March 2011. Data for the follow up PPS in September 2011 were collected as part of a national PPS of healthcare associated infection and antimicrobial use developed using ECDC protocols.
Results
In the baseline PPS data were collected in 22 (56%) acute hospitals. The frequency of recording the reason for treatment in medical notes was similar in Scotland (75.9%) and Europe (75.7%). Compliance with policy (81.0%) was also similar to Europe (82.5%) but duration of surgical prophylaxis <24hr (68.6%), was higher than in Europe (48.1%, OR: 0.41, p<0.001). Following the development and implementation of the prescribing indicators monthly measurement and data feedback in admission units illustrated improvement in indication documented of ≥90% and compliance with antibiotic prescribing policy increasing from 76% to 90%. The initial prescribing indicator in surgical prophylaxis was less successful in providing consistent national data as there was local discretion on which procedures to include. Following a review and a focus on colorectal surgery the mean proportion receiving single dose prophylaxis exceeded the target of 95% and the mean proportion compliant with policy was 83%. In the follow up PPS of 2011 indication documented (86.8%) and policy compliant (82.8%) were higher than in baseline PPS.
Conclusions
The baseline PPS identified priorities for quality improvement. SAPG has demonstrated that implementation of regularly reviewed national prescribing indicators, acceptable to clinicians, implemented through regular systematic measurement can drive improvement in quality of antibiotic use in key clinical areas. However, our data also show that the ESAC PPS method may underestimate the proportion of surgical prophylaxis with duration <24hr.
doi:10.1186/2047-2994-2-3
PMCID: PMC3573889  PMID: 23320479
Antimicrobial stewardship; Quality improvement; Prescribing indicators; Point prevalence survey; Antibiotic; Hospital prescribing; Surgical prophylaxis
2.  Outbreak of Clostridium difficile PCR ribotype 027 - the recent experience of a regional hospital 
BMC Infectious Diseases  2014;14:209.
Background
Clostridium difficile infection (CDI) is the leading cause of healthcare-associated diarrhea, and several outbreaks with increased severity and mortality have been reported. In this study we report a C. difficile PCR ribotype 027 outbreak in Portugal, aiming to contribute to a better knowledge of the epidemiology of this agent in Europe.
Methods
Outbreak report with retrospective study of medical records and active surveillance data of all inpatients with the diagnosis of CDI, from 1st January to 31th December 2012, in a Portuguese hospital. C. difficile isolates were characterized regarding ribotype, toxin genes and moxifloxin resistance. Outbreak control measures were taken, concerning communication, education, reinforcement of infection control measures, optimization of diagnosis and treatment of CDI, and antibiotic stewardship.
Results
Fifty-three inpatients met the case definition of C. difficile-associated infection: 55% males, median age was 78.0 years (interquartile range: 71.0-86.0), 75% had co-morbidities, only 15% had a nonfatal condition, 68% had at least one criteria of severe disease at diagnosis, 89% received prior antibiotherapy, 79% of episodes were nosocomial. CDI rate peak was 13.89/10,000 bed days. Crude mortality rate at 6 months was 64.2% while CDI attributable cause was 11.3%. Worse outcome was related to older age (P = 0.022), severity criteria at diagnosis (leukocytosis (P = 0.008) and renal failure), and presence of fatal underlying condition (P = 0.025). PCR ribotype 027 was identified in 16 of 22 studied samples.
Conclusions
This is the first report of a 027-CDI outbreak in Portugal. We emphasize the relevance of the measures taken to control the outbreak and highlight the importance of implementing a close and active surveillance of CDI.
doi:10.1186/1471-2334-14-209
PMCID: PMC3998949  PMID: 24739945
Clostridium difficile; Outbreak; PCR ribotype 027; Portugal
3.  Understanding the Determinants of Antimicrobial Prescribing Within Hospitals: The Role of “Prescribing Etiquette” 
Prescribing etiquette is an important determinant of antimicrobial prescribing behaviors. Prescribing etiquette recognizes clinical decision-making autonomy and the role of hierarchy in influencing practice. Existing clinical groups and clinical leadership should be utilized to influence antimicrobial prescribing behaviors.
Background. There is limited knowledge of the key determinants of antimicrobial prescribing behavior (APB) in hospitals. An understanding of these determinants is required for the successful design, adoption, and implementation of quality improvement interventions in antimicrobial stewardship programs.
Methods. Qualitative semistructured interviews were conducted with doctors (n = 10), pharmacists (n = 10), and nurses and midwives (n = 19) in 4 hospitals in London. Interviews were conducted until thematic saturation was reached. Thematic analysis was applied to the data to identify the key determinants of antimicrobial prescribing behaviors.
Results. The APB of healthcare professionals is governed by a set of cultural rules. Antimicrobial prescribing is performed in an environment where the behavior of clinical leaders or seniors influences practice of junior doctors. Senior doctors consider themselves exempt from following policy and practice within a culture of perceived autonomous decision making that relies more on personal knowledge and experience than formal policy. Prescribers identify with the clinical groups in which they work and adjust their APB according to the prevailing practice within these groups. A culture of “noninterference” in the antimicrobial prescribing practice of peers prevents intervention into prescribing of colleagues. These sets of cultural rules demonstrate the existence of a “prescribing etiquette,” which dominates the APB of healthcare professionals. Prescribing etiquette creates an environment in which professional hierarchy and clinical groups act as key determinants of APB.
Conclusions. To influence the antimicrobial prescribing of individual healthcare professionals, interventions need to address prescribing etiquette and use clinical leadership within existing clinical groups to influence practice.
doi:10.1093/cid/cit212
PMCID: PMC3689346  PMID: 23572483
prescribing etiquette; antimicrobial prescribing; prescribing behavior
4.  Covering more Territory to Fight Resistance: Considering Nurses’ Role in Antimicrobial Stewardship 
The potential contribution nurses can make to the management of antimicrobials within an in-patient setting could impact on the development of antimicrobial resistance (AMR) and healthcare associated infections (HCAIs). Current initiatives promoting prudent antimicrobial prescribing and management have generally failed to include nurses, which subsequently limits the extent to which these strategies can improve patient outcomes. For antimicrobial stewardship (AS) programmes to be successful, a sustained and seamless level of monitoring and decision making in relation to antimicrobial therapy is needed. As nurses have the most consistent presence as patient carer, they are in the ideal position to provide this level of service. However, for nurses to truly impact on AMR and HCAIs through increasing their profile in AS, barriers and facilitators to adopting this enhanced role must be contextualised in the implementation of any initiative.
doi:10.1177/1757177410389627
PMCID: PMC3083718  PMID: 21532974
Antimicrobial drug resistance; nurse; healthcare associated infection; Clostridium difficile
5.  Antimicrobial stewardship in long term care facilities: what is effective? 
Intense antimicrobial use in long term care facilities promotes the emergence and persistence of antimicrobial resistant organisms and leads to adverse effects such as C. difficile colitis. Guidelines recommend development of antimicrobial stewardship programs for these facilities to promote optimal antimicrobial use. However, the effectiveness of these programs or the contribution of any specific program component is not known. For this review, publications describing evaluation of antimicrobial stewardship programs for long term care facilities were identified through a systematic literature search. Interventions included education, guidelines development, feedback to practitioners, and infectious disease consultation. The studies reviewed varied in types of facilities, interventions used, implementation, and evaluation. Comprehensive programs addressing all infections were reported to have improved antimicrobial use for at least some outcomes. Targeted programs for treatment of pneumonia were minimally effective, and only for indicators of uncertain relevance for stewardship. Programs focusing on specific aspects of treatment of urinary infection – limiting treatment of asymptomatic bacteriuria or prophylaxis of urinary infection – were reported to be effective. There were no reports of cost-effectiveness, and the sustainability of most of the programs is unclear. There is a need for further evaluation to characterize effective antimicrobial stewardship for long term care facilities.
doi:10.1186/2047-2994-3-6
PMCID: PMC3931475  PMID: 24521205
Long term care facility; Antimicrobial stewardship; Pneumonia; Urinary tract infection
6.  Antimicrobial susceptibility profiles of human and piglet Clostridium difficile PCR-ribotype 078 
In the last decade, outbreaks of nosocomial Clostridium difficile infections (CDI) occurred worldwide. A new emerging type, PCR-ribotype 027, was the associated pathogen. Antimicrobial susceptibility profiles of this type were extensively investigated and used to partly explain its spread. In Europe, the incidence of C. difficile PCR-ribotype 078 recently increased in humans and piglets. Using recommendations of the European Committee on Antimicrobial Susceptibility Testing (EUCAST) and the Clinical and Laboratory Standards Institute (CLSI) we studied the antimicrobial susceptibility to eight antimicrobials, mechanisms of resistance and the relation with previously prescribed antimicrobials in human (n=49) and porcine (n=50) type 078 isolates. Human and porcine type 078 isolates showed similar antimicrobial susceptibility patterns for the antimicrobials tested. In total, 37% of the isolates were resistant to four or more antimicrobial agents. The majority of the human and porcine isolates were susceptible to amoxicillin (100%), tetracycline (100%) and clindamycin (96%) and resistant to ciprofloxacin (96%). More variation was found for resistance patterns to erythromycin (76% in human and 59% in porcine isolates), imipenem (29% in human and 50% in porcine isolates) and moxifloxacin (16% for both human and porcine isolates). MIC values of cefuroxim were high (MICs >256 mg/L) in 96% of the isolates. Resistance to moxifloxacin and clindamycin was associated with a gyr(A) mutation and the presence of the erm(B) gene, respectively. A large proportion (96%) of the erythromycin resistant isolates did not carry the erm(B) gene. The use of ciprofloxacin (humans) and enrofloxacin (pigs) was significantly associated with isolation of moxifloxacin resistant isolates. Increased fluoroquinolone use could have contributed to the spread of C. difficile type 078.
doi:10.1186/2047-2994-2-14
PMCID: PMC3651393  PMID: 23566553
7.  Clostridium difficile exposure as an insidious source of infection in healthcare settings: an epidemiological model 
BMC Infectious Diseases  2013;13:376.
Background
Clostridium difficile is the leading cause of infectious diarrhea in hospitalized patients. Its epidemiology has shifted in recent years from almost exclusively infecting elderly patients in whom the gut microbiota has been disturbed by antimicrobials, to now also infecting individuals of all age groups with no recent antimicrobial use.
Methods
A stochastic mathematical model was constructed to simulate the modern epidemiology of C. difficile in a healthcare setting, and, to compare the efficacies of interventions.
Results
Both the rate of colonization and the incidence of symptomatic disease in hospital inpatients were insensitive to antimicrobial stewardship and to the prescription of probiotics to expedite healthy gut microbiota recovery, suggesting these to be ineffective interventions to limit transmission. Comparatively, improving hygiene and sanitation and reducing average length of stay more effectively reduced infection rates. Although the majority of new colonization events are a result of within-hospital ward exposure, simulations demonstrate the importance of imported cases with new admissions.
Conclusions
By analyzing a wide range of screening sensitivities, we identify a previously ignored source of pathogen importation: although capturing all asymptomatic as well as symptomatic introductions, individuals who are exposed but not yet colonized will be missed by even a perfectly sensitive screen on admission. Empirical studies to measure the duration of this latent period of infection will be critical to assessing C. difficile control strategies. Moreover, identifying the extent to which the exposed category of individual contributes to pathogen importation should be explicitly considered for all infections relevant to healthcare settings.
doi:10.1186/1471-2334-13-376
PMCID: PMC3751620  PMID: 23947736
8.  Risk Factors for Recurrence of Clostridium difficile Infection: Effect of Vancomycin-resistant Enterococci Colonization 
Journal of Korean Medical Science  2011;26(7):859-864.
Recurrent Clostridium difficile infection (CDI) is one of the most difficult problems in healthcare infection control. We evaluated the risk factors associated with recurrence in patients with CDI. A retrospective cohort study of 84 patients with CDI from December 2008 through October 2010 was performed at Pusan National University Yangsan Hospital. Recurrence occurred in 13.1% (11/84) of the cases and in-hospital mortality rate was 7.1% (6/84). Stool colonization with vancomycin-resistant enterococci (VRE) (P = 0.006), exposure to more than 3 antibiotics (P = 0.009), low hemoglobin levels (P = 0.025) and continued use of previous antibiotics (P = 0.05) were found to be more frequent in the recurrent group. Multivariate analysis indicated that, stool VRE colonization was independently associated with CDI recurrence (odds ratio, 14.519; 95% confidence interval, 1.157-182.229; P = 0.038). This result suggests that stool VRE colonization is a significant risk factor for CDI recurrence.
doi:10.3346/jkms.2011.26.7.859
PMCID: PMC3124713  PMID: 21738336
Clostridium difficile; Recurrence; Risk factors; VRE
9.  Evaluation of Programmatic Changes to an Antimicrobial Stewardship Program with House Officer Feedback 
Rationale, aims and objectives
A collegial relationship between prescribers and antimicrobial stewards, along with an appreciation of the importance of antimicrobial stewardship, is essential for optimal functioning of an antimicrobial stewardship program (ASP). Programmatic adjustments based on feedback may be beneficial to the success of ASPs. The objective of this study is to assess the experience of house officers with the antimicrobial stewardship program (ASP) and the effect of programmatic improvements.
Methods
A survey of house officers at an academic medical center was conducted assessing their experience with the ASP before (2008) and after (2010) programmatic interventions were instituted.
Results
Of 225 house officer surveys sent, we received 97 responses (88% from MD’s). The majority indicated that ASP was either very or somewhat important in fighting antibiotic resistance (100%), improving patient care (97%), preventing medication errors (91%), and containing healthcare costs (89%). Ninety-one percent indicated either a very good or good educational experience with the ASP. The ASP often reminded respondents of a patient’s allergy (31%), to adjust for renal function (78%), and 38% were prevented from making a medication error. Comparing 2008 and 2010, a higher proportion of respondents in 2010 said they had a very good or good educational experience with ASP (84% vs 98%, OR=8.40, P=0.022) and a lower proportion of respondents reported confusion about ASP procedures (59% vs 39%, OR=0.43, P=0.048).
Conclusions
House officer feedback resulted in ASP policy changes which improved the ASP experience.
doi:10.1111/j.1365-2753.2012.01840.x
PMCID: PMC3381855  PMID: 22420938
Antimicrobial Stewardship; Quality improvement; House Officer Feedback
10.  Antimicrobial Stewardship Programs in Health Care Systems 
Clinical Microbiology Reviews  2005;18(4):638-656.
Antimicrobial stewardship programs in hospitals seek to optimize antimicrobial prescribing in order to improve individual patient care as well as reduce hospital costs and slow the spread of antimicrobial resistance. With antimicrobial resistance on the rise worldwide and few new agents in development, antimicrobial stewardship programs are more important than ever in ensuring the continued efficacy of available antimicrobials. The design of antimicrobial management programs should be based on the best current understanding of the relationship between antimicrobial use and resistance. Such programs should be administered by multidisciplinary teams composed of infectious diseases physicians, clinical pharmacists, clinical microbiologists, and infection control practitioners and should be actively supported by hospital administrators. Strategies for changing antimicrobial prescribing behavior include education of prescribers regarding proper antimicrobial usage, creation of an antimicrobial formulary with restricted prescribing of targeted agents, and review of antimicrobial prescribing with feedback to prescribers. Clinical computer systems can aid in the implementation of each of these strategies, especially as expert systems able to provide patient-specific data and suggestions at the point of care. Antibiotic rotation strategies control the prescribing process by scheduled changes of antimicrobial classes used for empirical therapy. When instituting an antimicrobial stewardship program, a hospital should tailor its choice of strategies to its needs and available resources.
doi:10.1128/CMR.18.4.638-656.2005
PMCID: PMC1265911  PMID: 16223951
11.  Growing a “Positive Culture” of Antimicrobial Stewardship in a Community Hospital 
Background:
Promoting the appropriate use of antimicrobials is a core value of antimicrobial stewardship. Prospective audit and feedback constitute an effective strategy for reducing the cost and use of antimicrobials, as well as their adverse effects, such as infection with Clostridium difficile.
Objective:
To evaluate the antimicrobial stewardship program in the intensive care unit at the authors’ hospital, in order to determine the cost and utilization of antimicrobials, as well as the rate of nosocomially acquired C. difficile infection.
Methods:
An infectious diseases team, consisting of a physician and a pharmacist, performed prospective audit and feedback during a pilot study (April to June 2010). The team met with the intensive care unit team daily to discuss optimization of therapy. The cost and utilization of antimicrobial drugs, as well as rates of C. difficile infection, were compared between the pilot period and the same period during the previous year (April to June 2009). For 3 months after the pilot phase (i.e., July to September 2010), the strategy was continued 3 days per week.
Results:
After introduction of the antimicrobial stewardship program, there was a significant reduction in the cost of antimicrobial drugs: $27 917 less than during the same period in the previous year, equivalent to a reduction of $15.45 (36.2%) per patient-day ($42.63 versus $27.18). Utilization of broad-spectrum antipseudomonal antimicrobial agents was also significantly lower, declining from 63.16 to 38.59 defined daily doses (DDDs) per 100 patient-days (reduction of 38.9%). After the pilot period, the rate declined further, to 28.47 DDDs/100 patient-days. During the pilot period, there were no cases of C. difficile infection, and in the post-pilot period, there was 1 case (overall rate 0.42 cases/1000 patient-days). This rate was lower than (but not significantly different from) the rate for April to September 2009 (1.87 cases/1000 patient-days). There were no differences in mortality rate or severity of illness.
Conclusion:
The antimicrobial stewardship program in this community hospital was associated with significant decreases in antimicrobial costs and in utilization of antipseudomonal antimicrobial agents and a nonsignificant decrease in the rate of C. difficile infection. Knowledge exchange, peer-to-peer communication, and decision support, key factors in this success, will be applied in implementing the antimicrobial stewardship program throughout the hospital.
PMCID: PMC3203822  PMID: 22479082
antimicrobial stewardship; prospective audit and feedback; Clostridium difficile; gestion responsable des antimicrobiens; vérification prospective et rétroaction; Clostridium difficile
12.  Importance of antimicrobial stewardship to the English National Health Service 
Antimicrobials are an extremely valuable resource across the spectrum of modern medicine. Their development has been associated with dramatic reductions in communicable disease mortality and has facilitated technological advances in cancer therapy, transplantation, and surgery. However, this resource is threatened by the dwindling supply of new antimicrobials and the global increase in antimicrobial resistance. There is an urgent need for antimicrobial stewardship (AMS) to protect our remaining antimicrobials for future generations. AMS emphasizes sensible, appropriate antimicrobial management for the benefit of the individual and society as a whole. Within the English National Health Service (NHS), a series of recent policy initiatives have focused on all aspects of AMS, including best practice guidelines for antimicrobial prescribing, enhanced surveillance mechanisms for monitoring antimicrobial use across primary and secondary care, and new prescribing competencies for doctors in training. Here we provide a concise summary to clarify the current position and importance of AMS within the NHS and review the evidence base for AMS recommendations. The evidence supports the impact of AMS strategies on modifying prescribing practice in hospitals, with beneficial effects on both antimicrobial resistance and the incidence of Clostridium difficile, and no evidence of increased sepsis-related mortality. There is also a promising role for novel diagnostic technologies in AMS, both in enhancing microbiological diagnosis and improving the specificity of sepsis diagnosis. More work is needed to establish an evidence base for interventions to improve public and patient education regarding the role of antibiotics in common clinical syndromes, such as respiratory tract infection. Future priorities include establishing novel approaches to antimicrobial management (eg, duration of therapy, combination regimens) to protect against resistance and working with the pharmaceutical industry to promote the development of new antimicrobials.
doi:10.2147/IDR.S39185
PMCID: PMC4047980  PMID: 24936131
antimicrobial resistance; antibiotics; National Health Service; methicillin-resistant Staphylococcus aureus; Clostridium difficile; prescribing
13.  In Vitro Evaluation of Antimicrobial Activity of Lactic Acid Bacteria against Clostridium difficile 
Toxicological Research  2013;29(2):99-106.
Clostridium difficile infection (CDI) has become a significant threat to public health. Although broad-spectrum antibiotic therapy is the primary treatment option for CDI, its use has evident limitations. Probiotics have been proved to be effective in the treatment of CDI and are a promising therapeutic option for CDI. In this study, 4 strains of lactic acid bacteria (LAB), namely, Lactobacillus rhamnosus (LR5), Lactococcuslactis (SL3), Bifidobacterium breve (BR3), and Bifidobacterium lactis (BL3) were evaluated for their anti-C. difficile activity. Co-culture incubation of C. difficile (106 and 1010 CFU/ml) with each strain of LAB indicated that SL3 possessed the highest antimicrobial activity over a 24-hr period. The cell-free supernatants of the 4 LAB strains exhibited MIC50 values between 0.424 mg/ml (SL3) and 1.318 (BR3) mg/ml. These results may provide a basis for alternative therapies for the treatment of C. difficile-associated gut disorders.
doi:10.5487/TR.2013.29.2.099
PMCID: PMC3834449  PMID: 24278635
Clostridium difficile infection; lactic acid bacteria; antimicrobial activity; cell-free supernatant
14.  Telehealth and Telecare: supporting unpaid carers in Scotland 
The Scottish Government Joint Improvement Team (JIT) and the Scottish Centre for Telehealth (SCT), now merged as the Scottish Centre for Telehealth and Telecare (SCTT), published an Education and Training Strategy for Telehealthcare in Scotland in March 2010. In implementing the Strategy’s dedicated Carers Workstream, the SCTT has been working with Carers Scotland and other carer organisations to promote awareness of the benefits of telehealth and telecare in helping to support unpaid carers. Following on from research undertaken by the University of Leeds into the benefits of telecare for carers, developments to date includes the publication of a Training Toolkit for professionals and carer organisations to assist with raising awareness of the benefits of telehealth and telecare specifically for unpaid carers. The toolkit includes outline training programmes, handouts, digital stories and case studies which all adaptable for local use. The presentation will provide an overview of the broader strategic carers’ agenda in relation to telehealth and telecare service delivery, an in-depth look at the Carers and Telehealthcare Training Toolkit and an update on an exciting new technology project to support young carers, being developed in collaboration with Princess Royal Trust for Carers, Glasgow Caledonian and Edinburgh Universities.
Project objectives/deliverables: Work with local authority, health boards and other partners to raise awareness of telehealth and telecare care amongst carers nationally and locally.Identify methods and programme for delivery to ensure that carers have access to appropriate information about access to telehealth and telecare services.Develop core content and supporting materials in carer awareness and telehealth and telecare training to form a Carers and Telehealthcare Training Toolkit.Evaluate impact of Telehealthcare Training Toolkit on staff and carers to inform future development of Toolkit contents.Incorporate telehealth and telecare for carers’ content into core curriculum and CPD modules for health and social care staff.Identify methods and programme for delivery to facilitate the integration of telehealth and telecare needs into carer, community care and health assessment processes.Work with Glasgow Caledonian University and partners to enhance young carers’ access to information and support via a technology solution.
PMCID: PMC3571193
unpaid carers; awareness raising; education; support; self-management
15.  The Impact of ICD-9-CM Code Rank Order on the Estimated Prevalence of Clostridium difficile Infections 
Current estimates of CDI prevalence in the US based on ICD-9-CM codes may be falsely elevated, indicating that a national standardized CDI surveillance system is warranted.
Background. US estimates of the Clostridium difficile infection (CDI) burden have utilized International Classification of Disease, Ninth Revision, Clinical Modification (ICD-9-CM) diagnosis codes. Whether ICD-9-CM code rank order affects CDI prevalence estimates is important because the National Hospital Discharge Survey (NHDS) and the Nationwide Inpatient Sample (NIS) have varying limits on the number of ICD-9-CM codes collected.
Methods. ICD-9-CM codes for CDI (008.45), C. difficile toxin assay results, and dates of admission and discharge were collected from electronic hospital databases for adult patients admitted to 4 hospitals in the United States from July 2000 through June 2006. CDI prevalence per 1000 discharges was calculated and compared for NHDS and NIS limits and toxin assay results from the same hospitals. CDI prevalence estimates were compared using the χ2 test, and the test of equality was used to compare slopes.
Results. CDI prevalence measured by NIS criteria was significantly higher than that measured using NHDS criteria (10.7 cases per 1000 discharges versus 9.4 cases per 1000 discharges; P < .001) in the 4 hospitals. CDI prevalence measured by toxin assay results was 9.4 cases per 1000 discharges (P = .57 versus NHDS). However, the CDI prevalence increased more rapidly over time when measured according to the NHDS criteria than when measured according to toxin assay results (β= 1.09 versus 0.84; P = .008).
Conclusions. Compared with the NHDS definition, the NIS definition captured 12% more CDI cases and reported significantly higher CDI rates. Rates calculated using toxin assay results were not different from rates calculated using NHDS criteria, but CDI prevalence appeared to increase more rapidly when measured by NHDS criteria than when measured by toxin assay results.
doi:10.1093/cid/cir246
PMCID: PMC3110281  PMID: 21653298
16.  Clostridium difficile infection in children hospitalized due to diarrhea 
The frequency of Clostridium difficile infection (CDI)-related hospitalizations is increasing. The aim of this study was to determine the extent of CDI among children hospitalized with diarrhea, risk factors or predictors for severe CDI, the prevalence of NAP1, and to compare the course of CDI depending on bacteria toxicity profile. A retrospective analysis of case records of 64 children (age range 3 months–16 years, median age 2.12 years) with CDI as defined by diarrheal disease and positive polymerase chain reaction (PCR) test (Xpert C. difficile) was conducted. Modified national adult guidelines were used to assess the severity of CDI. CDIs represented 2.7 % of patients with diarrhea (13.5 cases per 1,000 admissions). Thirty-three CDIs (52 %) were community-associated. Antibacterial use preceded CDI in 61 patients (95 %). Seventeen cases (27 %) were binary toxin-positive (CDT+), 13 of which were NAP1 (20.5 %). Over 75 % of CDIs with NAP1 was hospital-acquired, and more often proceeded with generalized infection (p < 0.05). Risk factors for severe CDI (34 %) included NAP1 [odds ratio (OR), 4.85; 95 % confidence interval (Cl), 1.23, 21.86) and co-morbidities (OR, 4.25; 95 % Cl, 1.34, 14.38). Diarrhea ≥10 stools daily was associated with severe CDI (p = 0.01). Recurrence occurred in three patients (4.5 %). There was no mortality. C. difficile is an important factor of antibiotic-associated diarrhea in children. Co-morbidities and NAP1 predispose to severe CDI.
doi:10.1007/s10096-013-1946-1
PMCID: PMC3907673  PMID: 24213847
17.  A multicenter study of Clostridium difficile infection-related colectomy, 2000–2006 
Background
The incidence of Clostridium difficile infection (CDI) has been increasing. Previous studies report that the number of colectomies for CDI is also rising. Outside of a few notable outbreaks, there are few published data documenting increasing severity of CDI. The specific aims of this multiyear, multicenter study were to assess CDI-related colectomy rates and compare CDI-related colectomy rates by CDI surveillance definition.
Methods
Cases of CDI and patients who underwent colectomy were identified electronically from 5 US tertiary-care centers from July 2000 through June 2006. Chart review was performed to determine if a colectomy was for CDI. Monthly CDI-related colectomy rates were calculated as the number of CDI-related colectomies per 1,000 CDI cases. Data between observational groups were compared using χ2 and Mann-Whitney U tests. Logistic regression was performed to evaluate risk factors for CDI-related colectomy.
Results
8569 cases of CDI were identified and 75 patients had CDI-related colectomy. The overall colectomy rate was 8.7/1,000 CDI cases. The CDI-related colectomy rate ranged from 0 to 23 per 1,000 CDI episodes across hospitals. The colectomy rates for healthcare facility (HCF)-onset CDI was 4.3/1000 CDI cases and 16.5 /1000 CDI cases for community-onset CDI (p <.05). There were significantly more CDI-related colectomies at hospitals B and C (p<.05).
Conclusions
The overall CDI-related colectomy rate was low, and there was no significant change in the CDI-related colectomy rate over time. Onset of disease outside of the study hospital was an independent risk factor for colectomy.
doi:10.1086/665318
PMCID: PMC3657463  PMID: 22476273
18.  Key research issues in Clostridium difficile 
Clostridium difficile is an emerging pathogen that causes C difficile-associated diarrhea, an important nosocomial infection. Control of this infection remains a challenge, and much needs to be determined about the antimicrobial resistance of the organism, antibiotic stewardship, contamination of the patient environment, and various host factors that determine susceptibility or resistance to infection. A national symposium focusing on C difficile infections, the Clostridium difficile Symposium on Emerging Issues and Research, was hosted on November 23, 2004, by the Department of Medical Microbiology and Infectious Diseases at the University of Manitoba, Winnipeg, Manitoba, in partnership with the Canadian Institutes of Health Research. This symposium, which aimed to summarize key research issues regarding C difficile infections in Canada, had the following objectives: to provide a forum for learning and discussion about C difficile and its impact on the health of Canadians; to identify the key research issues that should be addressed; and to explore potential research funding opportunities and collaboration. The present report summarizes key research issues identified for C difficile infections in Canada by addressing four major themes: diagnosis and surveillance, infection prevention and control, antibiotic stewardship, and clinical management.
PMCID: PMC2095041  PMID: 18159559
Clostridium difficile; Diarrhea; Research issues
19.  Defining acute renal dysfunction as a criterion for the severity of Clostridium difficile infection in patients with community-onset vs hospital-onset infection 
The Journal of hospital infection  2013;83(4):294-299.
SUMMARY
Background
Acute renal dysfunction can be used to define severe Clostridium difficile infection (CDI). The Society for Healthcare Epidemiology of America (SHEA) and Infectious Disease Society of America (IDSA) guidelines define acute renal dysfunction as serum creatinine (SrCr) ≥1.5 times the premorbid level.
Aim
To determine the ability to assess premorbid SrCr in hospitalized patients with CDI, stratified into community-onset CDI (CO-CDI) and hospital-onset CDI (HO-CDI); and to evaluate differing definitions for premorbid SrCr as a criterion for acute renal dysfunction.
Methods
Hospitalized patients with CDI were stratified into CO-CDI and HO-CDI. The ability to assess premorbid SrCr was determined, and the incidence of acute renal dysfunction and the severity of CDI were compared using varying definitions of premorbid SrCr.
Findings
In total, 293 patients with CDI were evaluated; of these, 135 (46%) had CO-CDI and 158 (54%) had HO-CDI. Premorbid SrCr data were not available for 37 (27%) patients with CO-CDI and one (<1%) patient with HO-CDI (P < 0.0001). Depending on the definition of premorbid SrCr used, acute renal dysfunction ranged from 17% to 24% for patients with CO-CDI (P = 0.26), and from 13% to 14% for HO-CDI (P = 0.81). The severity of CDI could not be determined for 43 out of 293 (15%) patients, primarily due to the lack of premorbid SrCr data (N = 38).
Conclusion
Assessment of acute renal dysfunction and the severity of CDI was not possible for many patients with CO-CDI using the current SHEA/IDSA guidelines. Given the increasing incidence of CO-CDI, an alternative definition of acute renal dysfunction may be required.
doi:10.1016/j.jhin.2012.12.011
PMCID: PMC3984400  PMID: 23433867
Healthcare-associated infections; Guideline development; Severity scoring systems; Clostridium difficile infection
20.  Clostridium difficile Infection in Hospitalized Liver Transplant Patients: A Nationwide Analysis 
Liver Transplantation  2012;18(8):972-978.
Introduction
Incidence of Clostridium difficile infection (CDI) is increasing among hospitalized patients. Liver transplant patients are at higher risk for acquiring CDI. Small, single-center studies, but no nation-wide analyses, have assessed this association.
Methods
We used the Healthcare Cost and Utilization Project- Nationwide Inpatient Sample (HCUP-NIS) from years 2004–2008 for this retrospective cross sectional study. Patients with any discharge diagnosis of liver transplant comprised the study population and were identified using ICD-9-CM codes. Those with a discharge diagnosis of CDI were considered cases. Our primary outcomes were prevalence of CDI and effect of CDI on inpatient mortality. Our secondary outcomes included length of stay and hospitalization charges. Regression analysis was used to derive odds ratios adjusted for potential confounders.
Results
There were 193,714 discharges with a diagnosis of liver transplant from 2004–2008. Prevalence of CDI was 2.7% in liver transplant population compared to 0.9% in non liver transplant population (p <0.001). Most of the liver transplant patients were in the 50–64 age group. Liver transplant patients were at higher odds of developing CDI (OR 2.88, 95% CI 2.68–3.10). Increasing age, increasing comorbidity, IBD and NG tube placement were also independent risk factors for CDI. CDI in liver transplant was associated with a higher mortality, 5.5% as compared to 2.3% in liver transplant only population (adjusted OR 1.7, 95% CI 1.3–2.2).
Conclusions
Liver transplant patients have a higher prevalence of CDI as compared to non liver transplant patients (2.7% vs. 0.9%).CDI was an independent risk factor for mortality in liver transplant population.
doi:10.1002/lt.23449
PMCID: PMC3405162  PMID: 22505356
Solid organ transplant; complications; outcomes research; cross sectional
21.  Assessing control bundles for Clostridium difficile: a review and mathematical model 
Clostridium difficile is the leading cause of infectious diarrhea in hospitalized patients. Integrating several infection control and prevention methods is a burgeoning strategy for reducing disease incidence in healthcare settings. We present an up-to-date review of the literature on ‘control bundles' used to mitigate the transmission of this pathogen. All clinical studies of control bundles reported substantial reductions in disease rates, in the order of 33%–61%. Using a biologically realistic mathematical model we then simulated the efficacy of different combinations of the most prominent control methods: stricter antimicrobial stewardship; the administering of probiotics/intestinal microbiota transplantation; and improved hygiene and sanitation. We also assessed the health gains that can be expected from reducing the average length of stay of inpatients. In terms of reducing the rates of colonization, all combinations had the potential to give rise to marked improvements. For example, halving the number of inpatients on broad-spectrum antimicrobials combined with prescribing probiotics or intestinal microbiota transplantation could cut pathogen carriage by two-thirds. However, in terms of symptomatic disease incidence reduction, antimicrobials, probiotics and intestinal microbiota transplantation proved substantially less effective. Eliminating within-ward transmission by improving sanitation and reducing average length of stay (from six to three days) yielded the most potent symptomatic infection control combination, cutting rates down from three to less than one per 1000 hospital bed days. Both the empirical and theoretical exploration of C. difficile control combinations presented in the current study highlights the potential gains that can be achieved through strategically integrated infection control.
doi:10.1038/emi.2014.43
PMCID: PMC4078791
epidemiology; healthcare-acquired infection; infection control bundle; transmission model; nosocomial; stochastic simulation
22.  Clostridium difficile infection in older adults 
Aging health  2013;9(4):403-414.
Clostridium difficile infection, the most frequent cause of nosocomial diarrhea, disproportionately affects older adults. The two most important risk factors for developing C. difficile infection are antimicrobial exposure and age >65 years old. Risk factors specific to older adults are frequent interactions with healthcare systems and age-related changes in physiology, including immune senescence and changes to the gut microbiome. Metronidazole and oral vancomcyin are the mainstays of conventional treatment for C. difficile infection. Alternative therapies include fidaxomicin, a narrow-spectrum macrocyclic antibiotic, and fectal bacteriotherapy, which offers an excellent therapeutic outcome. Strategies to prevent C. difficile infections include enhanced infection control measures and reducing inappropriate antimicrobial use through stewardship.
doi:10.2217/ahe.13.37
PMCID: PMC4061705  PMID: 24955106
aging; antimicrobial stewardship; Clostridium difficile infection; fecal bacteriotherapy; fidaxomicin; infection control; long-term care facilities; metronidzole; older adults; vancomycin
23.  Hospital-Associated Clostridium difficile Infection: Is It Necessary to Track Community-Onset Disease? 
Objectives
Compare Clostridium difficile infection (CDI) rates using a traditional definition [i.e. diagnosed > 48 hours after admission, healthcare-onset CDI (HO/CDI)] versus expanded definitions, including both HO/CDI cases and community-onset CDI cases diagnosed ≤ 48 hours from admission who were hospitalized in the previous 30 or 60 days [healthcare facility-associated (HCFA)-30 and HCFA-60]. Determine if differences exist between patients with CDI onset in the community versus healthcare setting.
Design
Prospective cohort
Setting
Tertiary acute-care facility.
Patients
Medicine patients diagnosed with CDI from 1/1/04 through 12/31/05.
Methods
CDI cases were classified as HO/CDI, HCFA-30, and/or HCFA-60. Patient demographics and medication exposures were obtained. The CDI incidence per the definitions, CDI rate variability, patient demographics, and medication exposures were compared.
Results
The HO/CDI rate (1.6 cases/1000 patient days) was significantly lower than the HCFA-30 (2.4) and the HCFA-60 (2.6) rates (p<0.01, both). There was good correlation between the HO/CDI rate and both the HCFA-30 and HCFA-60 rates (correlation=0.69 and 0.70, p<0.01 both). There were no months where the CDI rate was > 3 SD from the mean. Patients with community-onset CDI were less likely to have received a fourth-generation cephalosporin (p=0.02) or IV vancomycin (p=0.01) while hospitalized.
Conclusions
Expanded definitions identify more patients with CDI. There is good correlation between traditional and expanded CDI definitions; therefore it is unclear if expanded surveillance is necessary to identify an abnormal change in CDI rates. Cases that met the expanded definitions were less like to have fourth-generation cephalosporin and vancomycin exposure.
doi:10.1086/596604
PMCID: PMC3598605  PMID: 19239377
Clostridium difficile; surveillance; hospitals
24.  Implementation of an antimicrobial stewardship program on the medical-surgical service of a 100-bed community hospital 
Background
Antimicrobial stewardship has been promoted as a key strategy for coping with the problems of antimicrobial resistance and Clostridium difficile. Despite the current call for stewardship in community hospitals, including smaller community hospitals, practical examples of stewardship programs are scarce in the reported literature. The purpose of the current report is to describe the implementation of an antimicrobial stewardship program on the medical-surgical service of a 100-bed community hospital employing a core strategy of post-prescriptive audit with intervention and feedback.
Methods
For one hour twice weekly, an infectious diseases physician and a clinical pharmacist audited medical records of inpatients receiving systemic antimicrobial therapy and made non-binding, written recommendations that were subsequently scored for implementation. Defined daily doses (DDDs; World Health Organization Center for Drug Statistics Methodology) and acquisition costs per admission and per patient-day were calculated monthly for all administered antimicrobial agents.
Results
The antimicrobial stewardship team (AST) made one or more recommendations for 313 of 367 audits during a 16-month intervention period (September 2009 – December 2010). Physicians implemented recommendation(s) from each of 234 (75%) audits, including from 85 of 115 for which discontinuation of all antimicrobial therapy was recommended. In comparison to an 8-month baseline period (January 2009 – August 2009), there was a 22% decrease in defined daily doses per 100 admissions (P = .006) and a 16% reduction per 1000 patient-days (P = .013). There was a 32% reduction in antimicrobial acquisition cost per admission (P = .013) and a 25% acquisition cost reduction per patient-day (P = .022).
Conclusions
An effective antimicrobial stewardship program was implemented with limited resources on the medical-surgical service of a 100-bed community hospital.
doi:10.1186/2047-2994-1-32
PMCID: PMC3499185  PMID: 23043720
Antimicrobial stewardship; ASP; Small community hospital
25.  National Institute of Allergy and Infectious Disease (NIAID) Funding for Studies of Hospital-Associated Bacterial Pathogens: Are Funds Proportionate to Burden of Disease? 
Background
Hospital-associated infections (HAIs) are associated with a considerable burden of disease and direct costs greater than $17 billion. The pathogens that cause the majority of serious HAIs are Enterococcus faecium, Staphylococcus aureus, Clostridium difficile, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species, referred as ESCKAPE. We aimed to determine the amount of funding the National Institute of Health (NIH) National Institute of Allergy and Infectious Diseases (NIAID) allocates to research on antimicrobial resistant pathogens, particularly ESCKAPE pathogens.
Methods
The NIH Research Portfolio Online Reporting Tools (RePORT) database was used to identify NIAID antimicrobial resistance research grants funded in 2007-2009 using the terms "antibiotic resistance," "antimicrobial resistance," and "hospital-associated infection."
Results
Funding for antimicrobial resistance grants has increased from 2007-2009. Antimicrobial resistance funding for bacterial pathogens has seen a smaller increase than non-bacterial pathogens. The total funding for all ESKCAPE pathogens was $ 22,005,943 in 2007, $ 30,810,153 in 2008 and $ 49,801,227 in 2009. S. aureus grants received $ 29,193,264 in FY2009, the highest funding amount of all the ESCKAPE pathogens. Based on 2009 funding data, approximately $1,565 of research money was spent per S. aureus related death and $750 of was spent per C. difficile related death.
Conclusions
Although the funding for ESCKAPE pathogens has increased from 2007 to 2009, funding levels for antimicrobial resistant bacteria-related grants is still lower than funding for antimicrobial resistant non-bacterial pathogens. Efforts may be needed to improve research funding for resistant-bacterial pathogens, particularly as their clinical burden increases.
doi:10.1186/2047-2994-1-5
PMCID: PMC3415121  PMID: 22958856
Antibiotic resistance; NIH; Hospital-associated infection; research funding; disease burden

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