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626 • CID 2009:48 (1 March) • SURFING THE WEB

S U R F I N G T H E W E B

I N V I T E D A R T I C L E

Victor L. Yu, Section Editor

Navigating the Web in Search of Resources on Antimicrobial

Stewardship in Health Care Institutions

Leonardo Pagani,1Inge C. Gyssens,2,3Benedikt Huttner,4Dilip Nathwani,5and Stephan Harbarth4

1Division of Infectious Diseases, Bolzano Central Hospital, Bolzano, Italy;2Nijmegen University Center for Infectious Diseases and Radboud University and3 Canisius-Wilhelmina Hospital, Nijmegen, The Netherlands;4Geneva University Hospitals and Medical School, Geneva, Switzerland; and5Ninewells Hospital and Medical School, Dundee, Scotland

Bacterial resistance to antimicrobials has become a public health threat for which coordinated action at the international, national, and local level is needed. Current recommendations for the control of antimicrobial overuse and resistance in hospitals recommend various strategies, including antimicrobial stewardship programs. Several of these integrated and mul-tidisciplinary antimicrobial management programs provide detailed information and recommendations on the Web. We performed a search of the most relevant and authoritative Web sites in English that were available without need for special registration or cost. The search excluded community-based programs, and we present only established programs or those providing expert information useful for building a hospital-based antimicrobial stewardship program. The overview of these Web sites may be useful either for institutions or individuals planning to implement such programs in their own health care institution or for educational purposes targeted at different professionals involved in improving antimicrobial practice.

Antibiotics are among the most commonly prescribed drugs in hospitals. Inappropriate use of these agents may have delete-rious consequences, because the emergence and dissemination of bacterial resistance is mainly driven by antibiotic selection pressure [1]. Despite many large-scale initiatives and campaigns at national and international level to promote more appropriate antibiotic use, no hospital or country in the world can claim to have resolved the problem of antibiotic misuse [2, 3].

Selection of the most appropriate antimicrobial treatment, optimization of drug dosing and duration of therapy needed to cure infection, improvement of patient safety through re-ducing the risk of toxicity and adverse effects, and control of resistant strains are the key principles of antimicrobial ste-wardship programs [4, 5]. Such institutional or nationwide comprehensive programs involve multiple strategies and co-operation among different professionals in health care, in a close alliance with infection control staff [6–8].

Received 17 October 2008; accepted 17 October 2008; electronically published 23 January 2009.

Reprints or correspondence: Dr. Stephan Harbarth, Infection Control Program, Geneva University Hospitals and Medical School, 1211 Geneva 14, Switzerland (harbarth @post.harvard.edu).

Clinical Infectious Diseases 2009; 48:626–32

 2009 by the Infectious Diseases Society of America. All rights reserved. 1058-4838/2009/4805-0018$15.00

DOI: 10.1086/596762

A Web search for the terms “antimicrobial/antibiotic ste-wardship” on a search engine such as Google easily retrieves

16000 hits. This review is not intended to summarize or

eval-uate the quality of all available Web-based resources related to antimicrobial stewardship programs. By identifying high-qual-ity and readily accessible resources, we have tried rather to supply some practical help for national focus groups involved in antibiotic policy making, for institutions or individuals plan-ning to implement such programs in their own health care institutions, or for educational and training purposes targeted at different professionals involved in improving antimicrobial practice. More specifically, we looked for practical information and Web sites covering the following areas and subjects:

1. Comprehensive Web sites, established by internationally recognized institutions, covering many different aspects of an-timicrobial stewardship.

2. Institutional Web sites from health care organizations with established antimicrobial stewardship programs that may help health care professionals implement similar programs at their own institutions.

3. Web sites from other societies and organizations with an emphasis on optimizing antimicrobial use in health care institutions.

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SURFING THE WEB • CID 2009:48 (1 March) • 627

SEARCH METHODS

We retrieved English-language Web sites that can be accessed without a special registration procedure, gathered on the basis of the authors’ personal files, along with an extensive Web search following cross-links from other Web pages. No attempt was made to perform a complete and systematic review of all available Web sites dealing with issues related to antimicrobial stewardship programs. Web sites were screened and selected according to the quality and ease of access to information on the basis of evaluations of the authors and the authoritativeness of or the degree of commercial relationship with the Web site sponsor(s).

The quality of the Web sites was determined by assessing the availability of comprehensive and up-to-date information, as was done elsewhere [9]. We did not include Web sites that redirected readers to recently published guidelines or to expert reviews that are easily retrievable through the PubMed database [7, 10–13]. Furthermore, we excluded Web sites that were not free of charge, were promotional in nature, did not offer in-formation in English, exclusively described antibiotic control in the community, or dealt only indirectly with antimicrobial stewardship–related issues. Sites sponsored solely by the phar-maceutical industry were excluded, as were sites that, in the opinion of the authors, did not fulfill the criteria of indepen-dence, comprehensiveness, and exhaustiveness. Finally, the key words “antimicrobial resistance (AMR) control” were not con-sidered a sufficient inclusion criterion, because Web sites deal-ing with control of antimicrobial resistance, in a broader sense, were recently reviewed in this journal [9, 14].

We particularly attempted to retrieve and highlight Web sites that had been generated by integrated antimicrobial steward-ship networks of health care professionals, according to the recently published guidelines of the Society for Healthcare Ep-idemiology of America–Infectious Diseases Society of America [7]. These networks may include, for instance, infectious dis-eases specialists, hospital pharmacists with infectious disdis-eases training, clinical microbiologists, clinical pharmacologists, in-formation system specialists, and hospital epidemiologists. For those Web sites that were inadvertently omitted in this review, please contact us via e-mail and provide a URL address and a brief overview of the site.

RESULTS

The search for and subsequent evaluation of important Web sites dealing with antimicrobial stewardship programs retrieved a large number of sites; therefore, an effort has been made to highlight only those of outstanding interest in the authors’ opinion. They are shown in tables 1 and 2, categorized into different areas and types of sponsors, as described in the in-troduction. In table 3, other interesting Web sites that do not

exclusively cover antimicrobial stewardship in healthcare are shown. Most of these sites cross-link to information containing interesting documents and presentations, points of view or other perspectives on antimicrobial stewardship program-re-lated issues. Many of them refer to the recently published IDSA-SHEA guidelines [7]; others include valuable independent con-tents. In all tables, we mention the source of information and the sponsor of the Web site, and we briefly summarize the content.

DISCUSSION

Web sites of outstanding interest. The following sites rep-resent in the authors’ opinion the best starting points for de-signing and implementing antimicrobial stewardship programs in health care institutions, regardless whether they are of local or national dimension. These sites provide, to different extents, guidelines, hospital or national antibiotic guides, clinical and diagnostic pathways, and pharmacy-related material, such as dosing, formulary restriction systems, or surveillance data on drug consumption.

The Centers for Disease Control and Prevention (http: //www.cdc.gov/drugresistance/healthcare/default.htm). This well-known site offers teaching material to download and many valuable tools, in languages in addition to English, including the “12 Steps to Prevent Antimicrobial Resistance among Hospitalized Adults” campaign. It should be consid-ered the cornerstone of antimicrobial stewardship programs in North America.

The Healthcare Infection Control Special Interest Group (http://www.asid.net.au/hicsigwiki/index.php?titlepAnti biotic_stewardship_programs#Guides). This site from Aus-tralia and New Zealand is rich with helpful information and teaching materials, provides a large number of related links, and represents a good example of multidisciplinary anti-microbial stewardship.

The Nebraska Medical Center (http://www.nebraskamed.com/ careers/education/asp/index.aspx). This is one of the best Web sites to provide information about the different aspects of an institutional antimicrobial stewardship program.

The Washington University in St. Louis and Barnes-Jewish Hospital (http://id2.wustl.edu/˜casabar/antibiotics.html). This site provides data on patterns of antimicrobial resistance, algorithms, and flow charts; is very rich in information about the antimicrobial stewardship program implemented; and may be very helpful to professionals who are willing to un-dertake such a program in their own institution. However, navigation of the institutional site is far from easy.

The “Antimicrobial Management Program” (http://www .uphs.upenn.edu/bugdrug/) of The University of Pennsyl-vania Health System (http://pennhealth.com). This very in-teresting and complete site covers many aspects of

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antimi-628 Table 1. Co mpre hensi ve W eb si tes fro m national or intern ational org anizations with in form ati on on ma ny asp ects of antimi cro bial st eward sh ip. Name of site or sponsor URL Ease of naviga ti on Pra ctical in -for m ati on fo r pro fes sion a ls Amou n t and scope of info rm ati on Tea chi ng mate ri al to dow n loa d Mater ial in mu ltip le langu a ge s Link s to oth e r W eb site s Cen ter s for Disea se Con tro l and Pr e ven ti on htt p :/ /ww w .c dc .g o v/ dr u g re s ista nce/ he a lth care /de faul t.h tm Excel len t Y es Larg e Y es Y es Y es The Pu bl ic Hea lth Age n c y of Ca nada htt p :/ /ww w .p h a c -a spc .g c .c a/ cipa rs -pi cra /link s -l ien s _e .ht m l Excel len t No A ver age Y es Y es Y es Healthcare Infection Control S pecial Interest Group http:// www .asid .net .au/ hicsigwiki/ index .php ?title p Ant ib iot ic _ste wa rd s hip _pro g rams Excel len t Y es Larg e Y es No Y es DeBug Infection Prevention Program http:// www .debug .net .au/ index .html Excellent Y es A verage Y e s N o Y es Ant ibi ot ic Res ista nc e Al lianc e Edu c ati on W iscon s in htt p :/ /ww w .a re ain iti ati ves .o rg Good No A ver age Y es No Y es Eur o pe a n Pro jec t Gro u p “AB S In ter n ati on a l” htt p :/ /ww w .a bs -i nt er n a tion a l.e u / Excel len t No A ver age No No Y es Antibiotic Resistance P revention and Control http:// www .abdn .ac .uk/ arpac/ Good No Small Y e s Y es Y e s The Scottish Government– Health and Community C are http:// www .scotland .gov .uk/ Publications/ 2 005/ 09/ 0 2132609/ 26099 Excellent Y es Large Y es N oY e s App rop ria te Ant ibi ot ic Pr e scri bi ng htt p :/ /ww w .d u n de e .a c .u k /facme d de n /APT /in de x .h tm Excel len t Y es Larg e Y es No Y es National Resource for Infection Control http:// www .nric .org .uk/ IntegratedCRD .nsf/ NRIC _Policy _Ant imi cro bi alPr e scri bi ng ?Op en F o rm Excel len t Y es Larg e No No Y es The Dut c h W or k ing Part y on Ant ibi ot ic Po licy htt p :/ /ww w .s wa b .n l/ swa b/ swabc ms .n s f/ sho wf s /for e ign Good Y es A ver age Y es Y es No

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629 Table 2. Inst itu tional W eb si tes with est ablish ed antimi cro bial st eward sh ip pro gra ms. Ins ti tu ti on or or g a niza tion URL Desig n and ease of naviga ti on Amou n t and scope of info rm ati on Tea chi ng mate ri al to dow n loa d Mater ial in mu ltip le langu a ge s Link s to ot he r W eb site s Qua lity Nebr a ska Med ical Cen te r htt p :/ /ww w .n e b ra skame d .c om /care e rs/ ed u c ation /asp/ In d ex .a spx Excel len t Larg e Y es No Y es Excel len t W ake Forest University Baptist Medical Center http:// www1 .wfubmc .edu/ id/ hosp/ Antimicrobial+Stewardship/ Excellent Large Y es No Y e s Excellen t The W ashington University in St. L ouis and Barnes-Jewish Hospital http:// id2 .wustl .edu/ ˜c asaba r/ ant ibi ot ics .h tm l A ver age Larg e Y es No Y es Good The Uni ver sit y of Pen n s ylvani a Hea lth Sy stem htt p :/ /ww w .u p h s .u p e n n .e du /bu g dr u g / Excel len t Larg e Y es No Y es Excel len t John s Hop k ins Med ical In sti tu tion s htt p :/ /ww w .h o p kin s -a bx gu ide .o rg /cme _cen ter .h tml htt p :/ /ww w .h o p kin sme d icine .o rg /AMP Excel len t Larg e Y es No Y es Excel len t Univ ers ity of Ke n tu c ky Cha nd ler Med ical Ce nt e r htt p :/ /ww w .h o s p .u k y .e d u /pha rm acy/ amt /de fa ult .h tm l Excel len t Larg e Y es No Y es Excel len t

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Table 3. Ot her W eb si tes of intere st for pers o ns comm itted to antimi cro bial st eward sh ip. Name of site or spo n s or URL Cou n tr y Guid el ine s News Edu c ation a l and te a chin g mate ri al Mater ial availabl e in mu ltip le langu a ge s Pr u d en t Ant ib iot ic User W ebs ite htt p :/ /ww w .p a us e -o n line .o rg .u k / Unit ed King d o m Y es No Y es No Cum br ia Natio na l Hea lth Syste m , Acut e Tr us t Ant ibio ti c Gui de line s htt p :/ /ww w .c um br iapc t.n h s .u k /med icine s mana ge m en t/ ant ibi oti c pr e scri bing gu ide line s/ 20 0 7 /hos pi ta lfr on tpa ge .a spx Unit ed King d o m Y es No Y es No Agency for Healthcare Research and Quality http:// www .ahrq .gov/ downloads/ pub/ e vidence/ pdf/ medigap/ medigap .pdf United States N o N o Y es No Acade m y fo r In fec ti on Mana ge me n t htt p :/ /ww w .i nf e cti on a cade my .o rg/ Unit ed Sta te s Y es Y es Y es No Pre m ier Inc . htt p :/ /ww w .p rem ier inc .c om /qu a lity -s afet y /too ls -s er vic es/ safe ty/ to p ics/ gui de line s /ot he r.j sp Unit ed Sta te s Y es No Y es No Bug s and Dr u g s —Ant im icro b ial Ref er e n c e Bo o k htt p :/ /ww w .b u g sand d ru gs .c a Cana da Y es No No No Amer ican Soc iet y of Hea lth -Sy ste m Pha rm acists htt p :/ /ww w .a shp .o rg /s _ashp /ind e x .a sp Unit ed Sta te s Y es Y es Y es No

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SURFING THE WEB • CID 2009:48 (1 March) • 631

crobial stewardship on the Web. It provides updated guidelines for antimicrobial therapy, discusses issues related to formulary restrictions, provides current susceptibility and clinical microbiology data, and discusses pharmacologic con-siderations for dose adjustments, and lists infection control procedures.

The DeBug Infection Prevention Program (http://www .debug.net.au/index.html). Although this Web site is mostly committed to infection control and prevention, it supports many aspects of antimicrobial stewardship programs, with downloadable examples of informative campaigns. Moreover, a computer-assisted antibiotic formulary and pharmacy order form is available.

Web sites with special information about antimicrobial ste-wardship programs. In this section, we describe some inter-esting Web sites that we found. These Web sites contain often practical information that may be also helpful for implemen-tation of antimicrobial stewardship programs.

The Public Health Agency of Canada (http://www.phac-aspc .gc.ca/cipars-picra/links-liens_e.html). Although it mainly fo-cuses on antimicrobial resistance and veterinary medicine, rather than on antimicrobial stewardship, this site provides several links to national or international institutions and agen-cies involved in pursuing multidisciplinary antibiotic poliagen-cies.

European Project “ABS International” (http://www.abs-international.eu/). This is the Web site of an international, multicenter project subsidized by the European Community that is run by a for-profit organization, which involves several European countries. Its aim is to share attitudes and knowl-edge about implementation of guidelines on antibiotic prac-tices. The Web site is still under construction and does not yet provide a huge amount of useful information.

Bugs and Drugs (http://www.bugsanddrugs.ca). This Cana-dian Web site is co-sponsored by Capital Health from the Alberta Health Services (http://www.capitalhealth.ca/default .htm) and the Canadian Committee on Antibiotic Resistance (http://www.ccar-ccra.com). Although it is not really com-mitted to antimicrobial stewardship programs, this interest-ing site provides the booklet “Bugs and Drugs,”, which con-tains a huge amount of information about antibiotic characteristics, indications, and restrictions, as well as infor-mation on microbiological issues. The last edition of the booklet was published in 2006, but corrections and updates are also available.

The Cumbria National Health System Acute Trust Antibiotic Guidelines (http://www.cumbriapct.nhs.uk/medicinesmanage ment/antibioticprescribingguidelines/2007/hospitalfrontpage .aspx). This Web site from United Kingdom not only offers detailed guidelines for antimicrobial prophylaxis and empir-ical treatment of adults, but it also links to some

pharmacy-related items. Although microbiology and infection control aspects are not thoroughly tackled, this represents a very interesting and useful Web site.

Prudent Antibiotic User Website (PAUSE) (http://www .pause-online.org.uk). This Web site from United Kingdom provides shared standardized teaching materials that aim to effect more prudent antimicrobial prescribing practices. It is particularly suited to the needs of undergraduate medical curriculum but can be adopted for postgraduate training. It is now also supported by the European Society of Clinical Microbiology and Infectious Diseases as a valued educational web site. It is a good Web site from an educational standpoint, although it lacks a comprehensive approach to all key aspects of stewardship.

The Dutch Working Party on Antibiotic Policy (SWAB) (http: //swab.nl). This site contains updated antibiotic guidelines formulated by experts in The Netherlands and encompasses the so-called NethMap project, an ongoing national surveil-lance system on the use of antimicrobial agents related to the prevalence of resistance to antimicrobials among the most important human pathogens. English-language contents are of average completeness, and teaching material is scanty.

Other Web sites of interest. In table 3, we describe other Web sites that do not present implemented or institutional an-timicrobial stewardship programs but, rather, documents that, in our opinion, could be worth a look. Some of them provide useful tools or take into account interesting aspects of antimi-crobial stewardship programs. The website of the Academy for Infection Management (http://www.infectionacademy.org), which is partly sponsored by the pharmaceutical industry, offers a rich resource library with case studies, guidelines, and other educational material. Finally, Johns Hopkins Medical Institutions now provide their high-quality antibiotic guidelines on the In-ternet (http://www.hopkinsmedicine.org/AMP).

Limitations. There are some limitations to our approach. Our exclusion of non–English language Web sites may have excluded high-quality resources from some non–English-speaking countries and probably introduces a bias toward programs from North America, Australia, and the United Kingdom. For instance, useful Web sites in French (e.g., the Web site for Antibiolor [http://www.antibiolor.org/site/ index.php]) or German (e.g., the Web site for AntiBiotika Strategien [http://www.antibiotika-strategien.at]) exist and may provide help for interested colleagues in Europe and elsewhere. We did not use other search engines, and this may have limited the number of hits we received. Finally, some antimicrobial stewardship programs may be immersed in in-fection control or prevention programs and, therefore, may not have appeared under our search terms.

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CONCLUSIONS

Internet resources have become important tools for getting information and advice on improving antimicrobial programs in everyday practice. In the era of high-level resistance of many hospital-acquired pathogens, a multidisciplinary approach is necessary: microbiologists, infectious diseases specialists, clin-ical pharmacists, and infection control experts should cooperate in antimicrobial stewardship programs. This brief review of easily accessible available resources on the Web may be helpful for anyone who is willing either to implement or to improve hospital-based antimicrobial stewardship programs or to educate hospital professionals about better antimicrobial practices.

Acknowledgments

We thank Catherine Dumartin, Dominique Monnet, Sara Cosgrove, Ronald Polk, Richard Drew, and Victor Yu for their critical comments and help in finding additional Web sites relevant to this article.

Financial support. A small, unrestricted grant was provided by the European Society of Clinical Microbiology and Infectious Diseases Study Group for Antibiotic Policies.

Potential conflicts of interest. All authors: no conflicts.

References

1. Harbarth S, Samore MH. Antimicrobial resistance determinants and future control. Emerg Infect Dis 2005; 11:794–801.

2. Goossens H, Guillemot D, Ferech M, et al. National campaigns to improve antibiotic use. Eur J Clin Pharmacol 2006; 62:373–9. 3. Harbarth S. Should the development of new antibiotics be a public

health priority? Curr Opin Crit Care 2007; 13:554–6.

4. MacDougall C, Polk RE. Antimicrobial stewardship programs in health care systems. Clin Microbiol Rev 2005; 18:638–56.

5. Fishman N. Antimicrobial stewardship. Am J Med 2006; 119:S53–61; discussion S62–70.

6. van Kasteren ME, Mannien J, Kullberg BJ, et al. Quality improvement of surgical prophylaxis in Dutch hospitals: evaluation of a multi-site intervention by time series analysis. J Antimicrob Chemother 2005; 56:1094–102.

7. Dellit TH, Owens RC, McGowan JE Jr, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance anti-microbial stewardship. Clin Infect Dis 2007; 44:159–77.

8. Agwu AL, Lee CK, Jain SK, et al. A World Wide Web–based antimi-crobial stewardship program improves efficiency, communication, and user satisfaction and reduces cost in a tertiary care pediatric medical center. Clin Infect Dis 2008; 47:747–53.

9. Harbarth S, Emonet S. Navigating the World Wide Web in search of resources on antimicrobial resistance. Clin Infect Dis 2006; 43:72–8. 10. Lesprit P, Brun-Buisson C. Hospital antibiotic stewardship. Curr Opin

Infect Dis 2008; 21:344–9.

11. Owens RC Jr. Antimicrobial stewardship: concepts and strategies in the 21st century. Diagn Microbiol Infect Dis 2008; 61:110–28. 12. Gould IM. Antibiotic policies to control hospital-acquired infection. J

Antimicrob Chemother 2008; 61:763–5.

13. Patel D, Lawson W, Guglielmo BJ. Antimicrobial stewardship pro-grams: interventions and associated outcomes. Expert Rev Anti Infect Ther 2008; 6:209–22.

14. Falagas ME, Karveli EA. World Wide Web resources on antimicrobial resistance. Clin Infect Dis 2006; 43:630–3.

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