RESEARCH
Best infection control practices for intradermal, subcutaneous, and intramuscular needle injections
Meilleures pratiques pour prévenir les infections liées aux injections intradermiques, sous-cutanées et intramusculaires
Prácticas óptimas contra las infecciones para las inyecciones intradérmicas, subcutáneas e intramusculares
Yvan HutinI, 1; Anja HauriII; Linda ChiarelloIII; Mary CatlinIV; Barbara StilwellII; Tesfamicael GhebrehiwetV; Julia GarnerII; the Members of the Injection Safety Best Practices Development Group
IMedical Officer, Department of Blood Safety and Clinical Technology, Health Technology and Pharmaceuticals, World Health Organization, 1211 Geneva 27, Switzerland (email: sign@who.int)
IIDepartment of Blood Safety and Clinical Technology, Health Technology and Pharmaceuticals, World Health Organization, Geneva, Switzerland
IIICenters for Disease Control and Prevention, Atlanta, GA, USA
IVUniversity of Arizona Cancer Center, Tucson, AZ, USA
VInternational Council of Nurses, Geneva, Switzerland
ABSTRACT
OBJECTIVE: To draw up evidence-based guidelines to make injections safer.
METHODS: A development group summarized evidence-based best practices for preventing injection-associated infections in resource-limited settings. The development process included a breakdown of the WHO reference definition of a safe injection into a list of potentially critical steps, a review of the literature for each of these steps, the formulation of best practices, and the submission of the draft document to peer review.
FINDINGS: Eliminating unnecessary injections is the highest priority in preventing injection-associated infections. However, when intradermal, subcutaneous, or intramuscular injections are medically indicated, best infection control practices include the use of sterile injection equipment, the prevention of contamination of injection equipment and medication, the prevention of needle-stick injuries to the provider, and the prevention of access to used needles.
CONCLUSION: The availability of best infection control practices for intradermal, subcutaneous, and intramuscular injections will provide a reference for global efforts to achieve the goal of safe and appropriate use of injections. WHO will revise the best practices five years after initial development, i.e. in 2005.
Keywords: Injections, Intradermal/adverse effects/standards; Injections, Subcutaneous/adverse effects/standards; Injections, Intramuscular/adverse effects/standards; Needles; Infection control/methods/standards; Benchmarking; Evidence-based medicine (source: MeSH, NLM).
RÉSUMÉ
OBJECTIF: Elaborer des lignes directrices à partir des meilleures données disponibles pour améliorer la sécurité des meilleures données disponibles pour améliorer la sécurité des injections.
MÉTHODES: Un groupe d'étude a recensé, à partir de données probantes, les meilleures pratiques permettant de prévenir les infections liées aux injections dans les situations de ressources limitées. Son travail a consisté à traduire la définition de référence de la sécurité des injections adoptée par l'OMS en une série d'étapes essentielles, à passer en revue l'ensemble des publications consacrées à chacune de ces étapes, à élaborer un projet de document sur les meilleures pratiques d'injection et à le soumettre à un examen collégial.
RÉSULTATS: La première chose à faire pour prévenir les infections associées aux injections est d'éliminer toutes les injections inutiles. Pour les injections intradermiques, sous-cutanées ou intramusculaires médicalement justifiées, il est recommandé d'utiliser du matériel d'injection stérile, de prévenir toute contamination du matériel d'injection et des produits injectés, d'éviter que le personnel ne se blesse en manipulant les aiguilles et d'empêcher l'accès aux aiguilles usagées.
CONCLUSION: Les meilleures pratiques pour la sécurité des injections intradermiques, sous-cutanées et intramusculaires serviront de référence pour les efforts mondiaux visant à garantir un usage sûr et approprié des injections. Ces meilleures pratiques seront révisées par l'OMS cinq ans après leur élaboration, soit en 2005.
Mots clés: Injection intradermique/effets indésirables/normes; Injection sous-cutanée/effets indésirables/normes; Injection intramusculaire/effets indésirables/normes; Aiguille; Lutte contre infection/méthodes/normes; Banc mesure performance; Médecine factuelle (source: MeSH, INSERM).
RESUMEN
OBJETIVO: Formular directrices basadas en la evidencia para aumentar la seguridad de las inyecciones.
MÉTODOS: Un grupo de desarrollo resumió las prácticas óptimas basadas en la evidencia para prevenir las infecciones asociadas a inyecciones en los entornos con recursos limitados. El proceso de desarrollo incluía un desglose de la definición de referencia de la OMS de lo que constituye una inyección segura en una lista de pasos potencialmente críticos, un examen de la literatura para cada uno de esos pasos, la formulación de las prácticas óptimas, y el examen por homólogos del documento preliminar.
RESULTADOS: La eliminación de las inyecciones innecesarias constituye la máxima prioridad para prevenir las infecciones asociadas a inyecciones. En el caso de las inyecciones intradérmicas, subcutáneas o intramusculares efectuadas por indicación médica, las mejores prácticas de control de las infecciones incluyen el uso de instrumental de inyección estéril, la prevención de la contaminación de dicho instrumental y de la medicación, la prevención de los pinchazos del dispensador, y la prevención del acceso a las agujas usadas.
CONCLUSIÓN: Las prácticas óptimas de control de las infecciones para las inyecciones intradérmicas, subcutáneas e intramusculares constituirán una referencia para los esfuerzos mundiales desplegados hacia la meta de la utilización segura y apropiada de las inyecciones. La OMS revisará las prácticas óptimas a los cinco años de iniciado su desarrollo, esto es, en 2005.
Palabras clave: Inyecciones intradérmicas/efectos adversos/normas; Inyecciones subcutáneas/efectos adversos/normas; Inyecciones intramusculares/efectos adversos/normas; Agujas; Control de infecciones/normas; Benchmarking; Medicina basada en evidencia (fuente: DeCS, BIREME).
Introduction
In transitional and developing countries where unnecessary injections are common, the average number of health care injections per person was estimated to be 3.7 per year (this includes all health care injections, including those given to diabetics for administering insulin) (1). Many injections, as well as being unnecessary, are also unsafe. Each year, the reuse of injection equipment may cause 20 million infections with hepatitis B virus (HBV), 2 million infections with hepatitis C virus (HCV), and 250 000 infections with human immunode ficiency virus (HIV) worldwide (1). These chronic infections lead to a high burden of morbidity and mortality (1).
No evidence-based guidelines are available to guide injection providers through the steps they should follow to prevent injection-associated infections. Thus, WHO asked a development group and a steering group to develop best practices for the use of safe injections (Box 1) using WHO-recommended processes to formulate evidence-based guidelines, as outlined below.
Methods
Intended users
The primary audience for the guidelines on best practice for safe injections includes public health professionals, clinicians, and infection control practitioners. The secondary audience includes injection providers reached through training or communications material developed on the basis of these best practices.
Definitions
The development group defined an injection as a procedure that introduces a substance into the body by piercing the skin or a mucosal membrane. Injections may be administered with a needle or with needleless devices, such as jet injectors. However, for the purpose of these best practices, only needle injections were considered. WHO defines a safe injection as one that does not harm the recipient, does not expose the provider to any avoidable risk, and does not result in waste that is dangerous to other people.
Analysis of the reference definition
The steering group separated this reference definition into 24 potentially critical issues (Table 1).
Review of evidence
The steering group searched the English language literature using MEDLINE. The search terms included injection(s), infection, sterilization, disinfection, vial, ampoule, medication, skin (preparation, cleaning, disinfection), hand hygiene, antisepsis, needle-stick(s), recapping, and sharps (container, collection, disposal). Identified articles were used to select additional key and MeSH terms for further searches. Relevant references in identified articles and additional studies made available by members of the development group were also reviewed.
Formulation of best practices
The steering group formulated best practices for each of the potentially critical issues identified. Best practices strongly supported by well-designed analytical, observational, or intervention studies were characterized as category I (Box 1). Those supported by theoretical rationale and suggestive, descriptive evidence were characterized as category II. Those recommended on the basis of expert consensus and theoretical rationale were characterized as category III. For several other practice issues, best practices were not formulated. However, guidance was formulated on the basis of expert consensus and theoretical rationale. The development group then reviewed a draft and disseminated it for public comment through SIGNpost, the electronic forum of the Safe Injection Global Network (SIGN). All comments obtained from this peer-review process were archived to keep a track of decisions made to modify, or not, the document. Finally, a summary was edited and reorganized so that it would be reader friendly and separate the best practices from the other practice issues.
Results
Analysis of available evidence preventing infections among injection recipients
Best infection control practices to prevent infections among injection recipients include the use of sterile injection equipment and the prevention of contamination of injection equipment and medication.
Use of sterile injection equipment
The most important infection control measures for preventing infection among injection recipients is the use of a sterile syringe and needle for each injection and to reconstitute each unit of medication (for medications that require a diluent). In many countries, the practice of reusing injection equipment in the absence of sterilization is common, and such practices have been associated with infections (1).
Use of a new, single-use syringe and needle provides the highest level of safety to the recipient. However, unreliable and insufficient supplies might lead to the equipment being reused (2). Even though boiling injection equipment for 20 min does not sterilize it (3), the use of pans to boil single-use injection equipment is common in developing and transitional countries. In many instances these pans are used as containers of tepid water where injection equipment is simply rinsed and soaked between injections (1). Although the use of injection equipment taken from damaged packages has not been associated with infection, it is necessary to use injection equipment that has been inspected for breaches in barrier integrity and to discard it if it is punctured, torn, or damaged.
When new single-use injection equipment is not available, equipment designed for sterilization can be used. Sterilizable injection equipment is now made of plastic that can be steam sterilized. A steam sterilization procedure includes initial cleaning, is conducted according to WHO recommendations (4), and is controlled using time, steam, and temperature (TST) spot indicators (3). Breakdowns in the management of hospitals and clinics lead to breaks in sterilization procedures (2). Health care systems that use sterilizable injection equipment have poorer injection safety records than those that use single-use equipment (5), and the use of sterilizable injection equipment has been specifically associated with infections (6, 7).
Preventing contamination of injection equipment and medication
Work environment. It is important to prepare injections in a clean designated area, where the risk of contamination by blood or body fluids is low. HBV persists for up to seven days on surfaces (8), which can potentially lead to environmental contamination. Environmental contamination is a potential source of HBV infection in settings where chronic haemodialysis is performed (8). Factors that might facilitate HBV transmission among patients receiving chronic haemodialysis include a high prevalence of HBV infection among patients, an environmental contamination with blood, a high frequency of percutaneous procedures, and the presence of patients with high levels of viraemia. These factors might also be found in other health care settings because of high HBV endemicity, limited implementation of standard precautions, overuse of injections, and the presence of people in whom the HBV replicates actively (e.g. children). In Romania, for example, where some of these conditions were present, HBV infection was associated with injections in 1998 (9). However, a review of injection practices in Romania suggested that single-use syringes and needles were not reused and that HBV transmission was probably related to the preparation of injections in environments that were potentially contaminated with blood or body fluids (10). The preparation of injections in contaminated environments might also lead to bacterial infection (11) and cause infections among drug users who inject (12).
Multi-dose vials. It is important to use single-dose vials rather than multi-dose vials whenever possible. Although preservatives reduce the survival of bacteria (13), multi-dose vials remain prone to bacterial contamination (11, 14, 15) and the use of multi-dose vials has been reported to be a potential source of infections in 19 studies (Table 2) (11, 14, 1632). In two episodes, a needle had been left in the septum of the vial (18, 23). Needles left in the septum of multi-dose vials might encourage the use of the same syringe to repeatedly draw medications for one patient, a practice that may lead to vial contamination (15) and infections among subsequent patients (23). Thus, if multi-dose vials must be used, it is essential that the person administering the injection pierces the septum with a sterile needle and it is important not to leave any needle in place in the stopper.
Breaking vials and ampoules. Injuries to injection providers can be another source of infection. While opening glass ampoules, providers may lacerate their hands (33), which can bleed and may cause infections (34). Thus, it is important to use pop-open ampoules rather than ampoules that need to be opened using a metal file, and to protect fingers with a clean barrier (e.g. small gauze pad) when opening ampoules that need a metal file to open.
Compromised packaging. Cracks and leaks in vials are a potential source of contamination (35). Although it is not known how effective a visual examination of the vial is in preventing infections, it is important to inspect the vial for and discard medications with visible contamination or breaches of integrity (e.g. cracks or leaks) and to follow product-specific recommendations for use, storage, and handling.
Aseptic techniques. Medical devices might become contaminated with bacteria if touched. Thus, a needle that has touched any non-sterile surface must be discarded.
Other practice issues
Provider's hand hygiene and skin integrity.Washing or disinfecting hands is a standard procedure that is carried out before preparing injection material. The need for hand hygiene between each injection will vary depending on the setting and on whether the health care worker has had contact with soil, blood, or body fluids. Injections have been administered in the absence of hand-washing and not caused infection among diabetic patients (36). Skin lesions and skin irritation are associated with bacterial contamination (37). Thus, it is necessary to avoid giving injections if skin integrity is compromised by local infection or other skin conditions (e.g. weeping dermatitis) and to cover any small cut.
Swabbing vial tops or ampoules. Swabbing vial tops or ampoules with an antiseptic or disinfectant is unnecessary (11, 38). Cotton balls and gauze stored wet in antiseptics might become contaminated and have contributed to infections among patients, particularly when benzalkonium chloride was used (16, 39, 40). Thus, if swabbing with an antiseptic is selected for use, a clean, single-use swab must be used and the product-specific recommended contact time must be adhered to. Cotton balls stored wet in a multi-use container must not be used.
Skin preparation of patient before injection. Although skin that is visibly soiled or dirty must be washed, swabbing the clean skin of a patient before giving an injection is unnecessary. Studies suggest that there is no increased risk of infection when injections were given in the absence of skin preparation (Table 3) (36, 38, 4144). Bacteria from the skin flora might be introduced through skin piercing (41). However, most of these bacteria are non-pathogenic and the number introduced is lower than the minimal infectious dose for pus formation (45). Skin-preparation protocols traditionally used, including wiping with 70% alcohol, may be insufficient to eliminate the skin flora because of a limited contact time (43, 46). While the benefit of skin preparation is unclear, unsafe skin preparation protocols may be harmful (39, 40). Thus, if swabbing with an antiseptic is selected for use, a clean, single- use swab must be used and the product-specific recommended contact time must be adhered to. Cotton balls stored wet in a multi-use container must not be used.
Analysis of available evidence preventing infections among injection providers
Injuries from sharp devices have been associated with the transmission of more than 40 pathogens, including HBV, HCV, and HIV (47, 48).
Prevention of needle-stick injuries to the provider
Best infection control practices for preventing infections among injection providers address the prevention of movements of patients, the prevention of unsafe recapping of needles, and the collection of contaminated sharps in puncture-proof and liquid-proof containers.
Movement of patients. Needle-stick injuries to providers when administering injections are usually attributable to the abrupt movement of patients during the procedure (48, 49). Thus, it is important that providers anticipate and take measures to prevent sudden patient movement during and after injection. In some instances, physical assistance from other health care workers or family members might help to ensure that the procedure is carried out under appropriate circumstances.
Recapping. Avoiding recapping of needles and other hand manipulations of used needles is essential for preventing needle-stick injuries. A high proportion of needle-stick injuries are attributable to two-handed recapping (48). Teaching the one-handed, scoopingresheathingrecapping technique was effective in reducing the risk of recapping-related needle-stick injuries in one study (50). Thus, it is essential to use the single- handed scoop technique if recapping is necessary (e.g. in circumstances where a sharps container is not available).
Sharps collection. It is important to collect and properly contain syringes and needles at the point of use in a sharps container that is puncture- and leak-proof and that is sealed before it is completely full. Unsafe sharps waste collection causes between 5% and 28% of needle-stick injuries (49, 51). Puncture- and liquid-proof containers designed for the collection of contaminated sharps are associated with a lower risk of needle-stick injuries than regular cardboard boxes (52). The presence of sharps containers close to the point of use reduces the incidence of recapping (53, 54) and of recapping-related needle-stick injuries (55, 56). Interventions that combine the provision of sharps containers and risk communications reduce the total number of needle-stick injuries (49, 57)
Other practice issues
Engineered technologies. Current hypodermic needles and syringes with safety features for preventing needle-stick injuries require a provider-dependent activation step. Their effectiveness is unclear (5860). None are able to protect the provider when giving an injection because the safety feature is only activated after use. Reports on the effectiveness of other, safer needle-bearing devices (e.g. intravenous catheters, phlebotomy needles) to protect health care personnel from needle-sticks are encouraging (6164). Thus, whenever possible, devices designed to prevent needle-stick injury that have been shown to be effective for patients and providers are preferable.
Analysis of available evidence preventing infections in the community
Contaminated sharps are a potential source of biohazard to the community at large. To prevent people being exposed to contaminated sharps, it is important to seal sharps containers for transport to a secure area in preparation for disposal (65). After closing and sealing, sharps containers must not be opened, emptied, reused, or sold. In South Asia, used injection equipment is sought for recycling, mostly for the plastic-ware industry (66). Such practices might lead to needle-stick injuries among waste pickers and can lead to illegal repackaging of syringes for reuse in hospitals and clinics. Finally, it is important to manage sharps waste in an efficient, safe, and environment-friendly way. Contaminated sharps were observed in the immediate surroundings of a high proportion of health care facilities in developing countries (5). Such unsafe sharps waste management exposes the community to needle-stick injuries (67).
Discussion
We used WHO-recommended processes to formulate best infection control practices for intradermal, subcutaneous, and intramuscular injections and to address the use of sterile injection equipment, the prevention of contamination of injection equipment and medication, the prevention of needle-stick injuries to the provider, and the prevention of access to used needles. In addition, we addressed other practical issues that are relevant to injection providers. Although we addressed the safety of injections from the perspectives of injection recipients, injection providers and communities, the burden of disease associated with unsafe injections is of a different magnitude among these three groups. In 2000, WHO estimated that contaminated injections might have caused 250 000 HIV infections among injection recipients, whereas needle-stick injuries might have caused 1000 HIV infections among injection providers. No estimates are available regarding the burden of disease among the general population associated with unsafe sharps waste disposal; however, the low frequency of needle-stick injuries in this group indicates that it would be of an even lower magnitude (68). Overall, making injection safe to the injection recipients should be the first priority from a public health point of view. Sharps waste management addresses a smaller burden of disease and may require the setting up of an infrastructure. Careful planning and integration throughout the health sector will limit costs and ensure sustainability.
The best practices do not constitute a standard for regulatory purposes or prescriptive guidelines. Rather, they distil critical steps believed to prevent injection-associated infections for resource-limited environments. Although this approach removes some elements that could make them directly applicable to a particular setting, it enables them to be adapted by specific programmes or countries on the basis of practicality, feasibility, or cost-effectiveness issues. For example, the recommendation to avoid multi-dose vials is not applicable in immunization services that make extensive use of them in developing countries. However, when multi-dose vials are used in immunization services, specific messages to providers will ensure their safe use.
These best practices did not address the use of specific safety devices, enabling the development group to avoid issues that could lead to actual or perceived conflicts of interest. Newer technologies supporting a safer use of injections have been developed. Auto-disable (AD) syringes inactivate after one use. Other safety mechanisms have been engineered to prevent needle-stick injuries. Policy decisions to recommend the use of these devices need to analyse in a cost-effectiveness evaluation the probability of achieving safe practices in the absence of the device, the effectiveness of the device in the setting where use is being considered, and the incremental cost involved.
These best practices do not include a recommendation to prepare the skin with an antiseptic. Skin-preparation protocols have an influence on the risk of infection for intravenous catheters (69). However, in this case, baseline rates of infections are higher and most infections are presumed to result from inward migration of bacteria from the insertion site (69). Among injecting drug users, skin cleaning may be associated with a lower risk of bacterial infections (41).
These best practices have several limitations. First, the scope of the best practice document was limited to intradermal, subcutaneous, and intramuscular injections that constitute the majority of injections and that are homogeneous in terms of infection control requirements. Second, because infections constitute the most common adverse effect associated with injections, the scope of these best practices was restricted to infection control and did not address other recommended practices (e.g. ensuring that the right dose of injection is given to the right patient, at the right time, etc.). Third, the quality of medications and equipment was not addressed, as it depends on national regulatory authorities rather than on injection providers. Fourth, in the absence of data, the practice of removing needles after injections to collect sharps waste separately was not addressed. Disassembling injection equipment might cause needle-stick injuries (48). In addition, it is unclear whether removing needles might produce splatters and aerosols as needle cutters do (70). Thus, safety evaluations are needed before this practice can be recommended. Fifth, although they call for a reduction in injection overuse, our best practices do not provide details regarding the strategies proven to be effective in reducing the use of injections. Additional details regarding the rational use of injections may be obtained from the WHO Department of Essential Drugs and Medicine Policy.
WHO will promote the use of these best practices to prevent injection-associated infections. Pictogrammes (Fig.1) were developed to illustrate each of the steps and are available for download from the following URL: www.injectionsafety.org. The best practices are also used as a reference for a set of WHO education tools and for a tool to assess injection safety in health care facilities. To ensure that these best practices continue to be useful, users should continue reviewing scientific literature for new information and WHO will plan for revisions using the same methodology five years after the initial development, i.e. in 2005. 
Acknowledgements
These best practices were approved by the steering group (who are the authors of this article), and the development group: Baheeja Abdulla (Infection Control Officer, Salaminya Medical Complex, Bahrain), Naima Al-Gasseer (Nursing and Midwife Services, WHO), Aranya Chaowalit (Dean, Faculty of Nursing, Prince of Songkla University, Thailand), Cynthia Chasokela (Director of Nursing Services, Ministry of Health and Child Welfare, Zimbabwe), John Nicolas Crofts (Deputy Director, Macfarlane Burnet Centre for Medical Research, Australia), Philippe Duclos (Immunization Safety, WHO), Pilar Gavinio (Hepatitis C Prevention, WHO), Catherine MacCaulay (Senior Quality Assurance Advisor, The Quality Assurance Project, USA), Henry Francis, Director, (Center on AIDS and Other Medical Consequences of Drug Abuse, National Institute on Drug Abuse, USA), Annette Pruess (Health Care Waste Management, WHO), and Arnaud Tarantola (Medical Officer, Groupe d'Etude sur le Risque d'Exposition des Soignants aux Agents infectieux (GERES), France).
Funding for the development of these best practices was provided by the United States Agency for International Development (USAID).
Conflicts of interest: none declared.
References
1. Hauri AM, Armstrong GL, Hutin YJF. Contaminated injections in health care settings. In: Ezzati M, Lopez AD, Rodgers A, Murray CJL, editors. Comparative quantification of health risks: global and regional burden of disease attributable to selected major risk factors. Geneva: World Health Organization; 2003.
2. Dicko M, Oni AQ, Ganivet S, Kone S, Pierre L, Jacquet B. Safety of immunization injections in Africa: not simply a problem of logistics. Bulletin of the World Health Organization 2000;78:163-9.
3. Sopwith W, Hart T, Garner P. Preventing infection from reusable medical equipment: A systematic review. BMC Infectious Diseases 2002;2:4. Available from:URL: http://www.biomedcentral.com
4. Immunization in practice. Module four: ensuring safe injections. Geneva: World Health Organization; 1998. WHO document WHO/EPI/TRAM/ 98.4.
5. Hofmann CA. The WHO injection safety assessment tool: First results. Presentation made at the annual meeting of the Safe Injection Global Network, 3031 August 2002, New Delhi, India. Geneva: World Health Organization; 2001. WHO document WHO/BCT/DCT/01.04.
6. Chen TZ, Wu JC, Yen FS, Sheng WY, Hwang SJ, Huo TI, et al. Injection with nondisposable needles as an important route for transmission of acute community-acquired hepatitis C virus infection in Taiwan. Journal of Medical Virology 1995;46:247-51.
7. Narendranathan M, Philip M. Reusable needles a major risk factor for acute virus B hepatitis. Tropical Doctor 1993;23:64-6.
8. Centers for Disease Control. Recommendations for preventing transmission of infections among chronic hemodialysis patients. Morbidity and Mortality Weekly Report 2001;50(RR05):1-43.
9. Hutin YJF, Craciun D, Ion-Neldelcu N, Mast EE, Alter MJ, Margolis HS. Using surveillance data to monitor key aspects of the epidemiology of hepatitis B virus (HBV) infection in Romania. Abstract presented at the annual meeting of the Infectious Diseases Society of America (IDSA). Denver (CO), November 1999.
10. Dentinger CM, Hutin YJF, Pasat L, Mihilescu I, Mast EE, Margolis HS. Knowledge and practices of nurses regarding injection safety and use of universal precautions, Vilcea district, Romania. Abstract presented at the annual meeting of the Society for Healthcare Epidemiology of America (SHEA). San Francisco (CA), April 1999 (Abstract S 42).
11. Simon PA, Chen RT, Elliot JA, Schwartz B. Outbreak of pyogenic abscesses after diphtheria and tetanus toxoids and pertussis vaccination. Pediatric Infectious Disease 1993;12:368-71.
12. Hagan H, Thiede H, Weiss NS, Hopkins SG, Duchin JS, Alexander ER. Sharing of drug preparation equipment as a risk factor for hepatitis C. American Journal of Public Health 2001;91:42-6.
13. Wallhaeusser, KH. [Praxis der Sterilisation, Desinfektion und Konservierung, 5th ed]. Stuttgart: Georg Thieme Verlag; 1995. In German.
14. Phillips G, Fleming LW, Stewart WK. The potential hazard of using multiple-dose heparin and insulin vials in continuous ambulatory peritoneal dialysis. Journal of Hospital Infection 1989;14:174-7.
15. Sheth NK, Post GT, Wisniewski TR, Uttech BV. Multidose vials versus single-dose vials: a study in sterility and cost-effectiveness. Journal of Clinical Microbiology 1983;17:377-9.
16. Nakashima AK, McCarthy MA, Martone WJ, Anderson RL. Epidemic septic arthritis caused by Serratia marcescens and associated with a benzalkonium chloride antiseptic. Journal of Clinical Microbiology 1987;25:1014-8.
17. Archibald LK, Ramos M, Arduino MJ, Aguero SM, Deseda C, Banerjee S, et al. Enterobacter cloacae and Pseudomonas aeruginosa polymicrobial bloodstream infections traced to extrinsic contamination of a dextrose multidose vial. Journal of Pediatrics 1998;133:640-4.
18. Oren I, Hershow RC, Ben-Porath E, Krivoy N, Goldstein N, Rishpon S, et al. A common-source outbreak of fulminant hepatitis B in a hospital. Annals of Internal Medicine 1989;110:691-8.
19. Borghans JGA, Standford JL. Mycobacterium chelonei in abscesses after injection of diphteria-pertussis-tetanus-polio-vaccine. American Review of Respiratory Disease 1973;107:1-8.
20. Inman, PM, Beck A, Brown, AE, Stanford, JL. Outbreak of injection abscesses due to Mycobacterium abscessus. Archives of Dermatology 1969;100:141-7.
21. Cabrera HA, Drake MA. An epidemic in a coronary care unit caused by Pseudomonas species. American Journal of Clinical Pathology 1975;64:700-4.
22. Greaves WL, Hinman AR, Facklam RR, Allman KC, Barret CL, Stetler HC. Streptococcal abscesses following diphtheria-tetanus toxoid-pertussis vaccination. Pediatric Infectious Disease 1982;1:388-90.
23. Kidd-Lunggren K, Broman E, Ekvall H, Gustavson O. Nosocomial transmission of hepatitis B virus infection through multiple-dose vials. Journal of Hospital Infection 1999;43:57-61.
24. Katzenstein TL, Jorgensen LB, Permin H, Hansen J, Nielsen C, Machuca R, et al. Nosocomial HIV-transmission in an outpatient clinic detected by epidemiological and phylogenetic analyses. AIDS 1999;13:1737-44.
25. Widell A, Christensson B, Wiebe T, Schalen C, Hansson HB, Allander T, et al. Epidemiologic and molecular investigation of outbreaks of hepatitis C virus infection on a pediatric oncology service. Annals of Internal Medicine 1999;130:130-4.
26. Massari M, Petrosillo N, Ippolito G, Solforosi L, Bonazzi L, Clementi M, et al. Transmission of hepatitis C virus in a gynecological surgery setting. Journal of Clinical Microbiology 2001;39:2860-3.
27. Black HJ. Plastic insulin syringes. BMJ 1988;296:1195.
28. Kothari T, Reyes MP, Brooks N. Pseudomonas cepacia septic arthritis due to intra-articular injections of methylprednisolone. Canadian Medical Association Journal 1977;116:1230,1232,1235.
29. Alter MJ, Ahtone J, Maynard JE. Hepatitis B virus transmission associated with a multiple-dose vial in a hemodialysis unit. Annals of Internal Medicine 1983;99:330-3.
30. Stetler HC, Garbe PL, Dwyer DM, Facklam RR, Orenstein WA, West GR, et al. Outbreaks of group A streptococcal abscesses following diphtheria-tetanus toxoid-pertussis vaccination. Pediatrics 1985;75:299-303.
31. Krause G, Whisenhunt S, Trepka M, Katz D, Nainan O, Wiersma S, et al. Patient- to-patient transmission of hepatitis C virus associated with use of multidose saline vials in a hospital. Presentation given at the 49th Annual Epidemic Intelligence Service (EIS) Conference. Atlanta (GA), 2000.
32. Grohskopf LA, Roth VR, Feikin DR, Arduino M, Carson L, Holt S, et al. Serratia liquefaciens bloodstream infections from contamination of epoetin alfa at a hemodialysis center. New England Journal of Medicine 2001;344:1491-7.
33. Parker MR. The use of protective gloves, the incidence of ampoule injury and the prevalence of hand laceration amongst anaesthetic personnel. Anaesthesia 1995;50:726-9.
34. Ross RS, Viazov S, Gross T, Hofmann F, Seipp HM, Roggendorf M. Transmission of hepatitis C virus from a patient to an anesthesiology assistant to five patients. New England Journal of Medicine 2000;343:1851-4.
35. Wang SA, Tokars JI, Biachine PJ, Carson LA, Arduino MJ, Smith AL, et al. Enterobacter cloacae bloodstream infections traced to contaminated human albumins. Clinical Infectious Diseases 2000;30:35-40.
36. Borders LM, Bingham PR, Riddle MC. Traditional insulin-use practices and the incidence of bacterial contamination and infection. Diabetes Care 1984;7:121-7.
37. Larson EL, Hughes CA, Pyrek JD, Sparks SM, Cagatay EU, Bartkus JM. Changes in bacterial flora associated with skin damage on hands of health care personnel. American Journal of Infection Control 1998;26:513-21.
38. Dann TC. Routine skin preparation before injection: an unnecessary procedure. Lancet 1969;2:96-8.
39. Sautter RL, Mattman LH, Legaspi RC. Serratia marcescens meningitis associated with a contaminated benzalkonium chloride solution. Infection Control 1984;5:223-5.
40. Reiss I, Borkhardt A, Füssle F, Sziegoleit A, Gortner L. Disinfectant contaminated with Klebsiella oxytoca as a source of sepsis in babies. Lancet 2000;356:310-1.
41. Binswanger IA, Kral AH, Bluthenthal RN, Rybold DJ, Edlin BR. High prevalence of abscesses and cellulitis among community-recruited injection drug users in San Francisco. Clinical Infectious Diseases 2000;30:579-81.
42. McCarthy JA, Covarrubias B, Sink P. Is the traditional alcohol wipe necessary before an insulin injection? Dogma disputed. Diabetes Care 1993;16:402.
43. Koivisto VA, Felig P. Is skin preparation necessary before insulin injection? Lancet 1978;1:1072-5.
44. Stepanas TV, Turley H, Tuohy EA. Reuse of disposable insulin syringes. Medical Journal of Australia 1982;1:311-3.
45. Elek, SD. Experimental staphylococcal infections in the skin of man. Annals of the New York Academy of Sciences 1956;56:85-90.
46. Selwyn S, Ellis H. Skin bacteria and skin disinfection reconsidered. BMJ 1972;1:136-40.
47. Collins CH, Kennedy DA. Microbiological hazards of occupational needle-stick and sharps injuries. Journal of Applied Bacteriology 1987;62:385-402.
48. Jagger J, Hunt EH, Brand-Elnaggar J, Pearson RD. Rates of needle-stick injury caused by various devices in a university hospital. New England Journal of Medicine 1988;319:284-8.
49. Haiduven DJ, DeMaio TM, Stevens DA. A five-year study of needle-stick injuries: significant reduction associated with communication, education, and convenient placement of sharps containers. Infection Control and Hospital Epidemiology 1992;3:265-71.
50. Froom P, Kristal-Boneh E, Melamed S, Shalom A, Ribak J. Prevention of needle-stick injury by the scooping-resheathing method. American Journal of Industrial Medicine 1998;34:15-9.
51. Khuri-Bulos NA, Toukan A, Mahafzah A, Al Adham M, Faori I, Abu Khader I, et al. Epidemiology of needle-stick and sharp injuries at a university hospital in a developing country: a 3-year prospective study at the Jordan University Hospital, 1993 through 1995. American Journal of Infection Control 1997;25:322-9.
52. Ribner BS, Landry MN, Gholson GL, Linden LA Impact of a rigid, puncture resistant container system upon needle-stick injuries. Infection Control 1987;8:63-6.
53. Makofsky D, Cone JE. Installing needle disposal boxes closer to the bedside reduces needle-recapping rates in hospital units. Infection Control and Hospital Epidemiology 1993;14:140-4.
54. Edmond M, Khakoo R, McTaggart B, Solomon R. Effect of bedside needle disposal units on needle recapping frequency and needle-stick injury. Infection Control and Hospital Epidemiology 1988;9:114-6.
55. Sellick JA Jr, Hazamy PA, Mylotte JM. Influence of an educational program and mechanical opening needle disposal boxes on occupational needle-stick injuries. Infection Control and Hospital Epidemiology 1991;12:725-31.
56. Linnemann CC Jr, Cannon C, DeRonde M, Lanphear B. Effect of educational programs, rigid sharps containers, and universal precautions on reported needle-stick injuries in healthcare workers. Infection Control and Hospital Epidemiology 1991;12:214-9.
57. Richard VS, Kenneth J, Ramaprabha P. Impact of introduction of sharps containers and of education programmes on the pattern of needle-stick injuries in a tertiary care centre in India. Journal of Hospital Infection 2001;47:163-5.
58. Younger B, Hunt EH, Robinson C, McLemore C. Impact of a shielded safety syringe on needle-stick injuries among health-care workers. Infection Control and Hospital Epidemiology 1992;13:349-53.
59. Orenstein R, Reynolds L, Karabaic M, Lamb A, Markowitz SM, Wong ES. Do protective devices prevent needle-stick injuries among health care workers? American Journal of Infection Control 1995;23:344-51.
60. Mulherin S, Rickman LS, Jackson MM. Initial worker evaluation of a new safety syringe. Infection Control and Hospital Epidemiology 1996;17:593-4.
61. Centers for Disease Control and Prevention. Evaluation of safety devices for preventing percutaneous injuries among health-care workers during phlebotomy procedures Minneapolis-St. Paul, New York City, and San Francisco, 19931995. Morbidity and Mortality Weekly Report 1997;46:21-5.
62. Chen LBY, Bailey E, Kogan G, Finkelstein LE, Mendelson MH. Prevention of needle-stick injuries in healthcare workers: 27 month experience with a resheathable safety winged steel needle using CDC NaSH Database. Infection Control and Hospital Epidemiology 2000;21:108.
63. Mendelson MH, Chen LBY, Finkelstein LE, Bailey E, Kogan G. Evaluation of a safety IV catheter (Insyte Autoguard, Becton Dickinson) using the Centers for Disease Control and Prevention (CDC) National Surveillance System for Hospital Healthcare Workers database. Infection Control and Hospital Epidemiology 2000;21:108.
64. Billiet LS, Parker CR, Tanley PC, Wallas CH. Needle-stick injury rate reduction during phlebotomy: A comparative study of two safety devices. Laboratory Medicine 1991;22:120-3.
65. Nielsen H, Rosthoj S, Machuca R, Nielsen C, Smith E. Nosocomial child-to-child transmission of HIV. Lancet 1998;352:1520.
66. Mujeeb SA, Adil MM, Altaf A, Hutin Y, Luby S. Recycling of injection equipment in Pakistan. Infection Control and Hospital Epidemiology 2003;24:145-6.
67. Liss GM, Crimi C, Jaczek KH, Anderson A, Slattery B, D'Cunha C. Improper office disposal of needles and other sharps: an occupational hazard outside of health care institutions. Canadian Journal of Public Health 1990;81:417-20.
68. The world health report 2002: reducing risks, promoting healthy life. Geneva: World Health Organization; 2002. p. 74.
69. Pearson ML. Guideline for prevention of intravascular device-related infections. The Hospital Infection Control Practices Advisory Committee. American Journal of Infection Control 1996;24:262-93.
70. Binley RJ, Fleming DO, Swift DL, Tepper BS. Release of residual material during needle cutting. American Journal of Infection Control 1984;12:282-8.
1 Correspondence should be addressed to this author.