On-line version ISSN 1680-5348
Print version ISSN 1020-4989
Rev Panam Salud Publica vol.30 n.6 Washington Dec. 2011
Ecosystem approach to promoting appropriate antibiotic use for children in indigenous communities in Ecuador
Enfoque ecosistémico de promoción del uso adecuado de antibióticos en niños de comunidades indígenas del Ecuador
Georgina MuñozI; Lorena MotaII; William R. BowieIII; Arturo QuizhpeIV; Elena OrregoII; Jerry M. SpiegelII; Annalee YassiV
IDivisión de Pediatría, Hospital Vicente Corral Moscoso, Cuenca, Ecuador
IIGlobal Health Research Program, College of Interdisciplinary Studies, University of British Columbia, Vancouver, British Columbia, Canada
IIIDivision of Infectious Diseases, Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada
IVFacultad de Ciencias Médicas, Universidad de Cuenca, Cuenca, Ecuador
VSchool of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada. Send correspondence to: Annalee Yassi, firstname.lastname@example.org
OBJECTIVE: To collect baseline data on infectious diseases and antibiotic use in two Andean indigenous communities in Ecuador in order to determine the feasibility and acceptability of applying an ecosystem approach to address associated problems.
METHODS: In visits to 65 households with children under age 5 years, environmental risk factors for infectious diseases were evaluated through rapid assessment. Caregivers' knowledge, attitudes, and practices related to antibiotic use were determined through a knowledge, practices, and coverage survey; antibiotic use was gleaned from inspection of medicine chests; and overall health of the 91 children (including nutritional status) was assessed. A workshop was held to share results and to craft a multicomponent intervention using an ecohealth framework.
RESULTS: Numerous environmental risk factors were identified, especially related to water and sanitation. Knowledge, attitudes, and practices revealed use of traditional and Western medicines and serious knowledge gaps. Antibiotics were present in 60.9% of households in Correuco and 46.8% in La Posta; malnutrition rates were 22.2% in Correuco and 26.1% in La Posta; diarrheic episodes were experienced in the previous month by 26.7% of children in Correuco and 47.8% in La Posta, with antibiotics prescribed in 50.0% and 47.1% of cases, respectively; and acute respiratory infections were incurred by 28.9% of children in Correuco and 47.8% in La Posta, with antibiotics prescribed in 53.8% and 50.0% of cases, respectively.
CONCLUSIONS: Environmental, social, and cultural factors must be addressed to prevent antibiotic resistance in addition to training health personnel. An ecosystem approach is well-suited for this goal.
Key words: Drug resistance, microbial; antibacterial agents; drug prescriptions; indigenous population; child, preschool; intervention studies; Ecuador.
OBJETIVO: Recopilar datos iniciales sobre las enfermedades infecciosas y el uso de antibióticos en dos comunidades indígenas andinas del Ecuador, con el objeto de determinar la factibilidad y la aceptabilidad de aplicar un enfoque ecosistémico para abordar los problemas asociados.
MÉTODOS: Mediante visitas a 65 hogares con niños menores de 5 años, se valoraron los factores de riesgo ambientales de las enfermedades infecciosas mediante una evaluación rápida. Se identificaron los conocimientos, las actitudes y las prácticas de los cuidadores relacionados con el uso de antibióticos por medio de una encuesta de conocimientos, prácticas y cobertura; el uso de antibióticos se dedujo a partir de la inspección de los botiquines; y se evaluó el estado general de salud de los 91 niños (incluido su estado de nutrición). Se organizó un taller para transmitir los resultados y para diseñar una intervención de múltiples componentes basada en un marco ecosistémico de la salud.
RESULTADOS: Se encontraron numerosos factores de riesgo ambientales, especialmente los relacionados con el agua y el saneamiento. El análisis del conocimiento, las actitudes y las prácticas reveló el uso de medicamentos tradicionales y occidentales, y profundas brechas de conocimiento. Había antibióticos en 60,9% de los hogares de Correuco y en 46,8% de La Posta; las tasas de desnutrición eran de 22,2% en Correuco y de 26,1% en La Posta; el mes anterior a la encuesta 26,7% de los niños de Correuco y 47,8% de los niños de La Posta habían tenido episodios de diarrea, con prescripción de antibióticos en 50,0% y 47,1% de los casos, respectivamente; y 28,9% de los niños de Correuco y 47,8% de los niños de La Posta habían tenido infecciones respiratorias agudas, con prescripción de antibióticos en 53,8% y 50,0% de los casos, respectivamente.
CONCLUSIONES: Deben abordarse los factores ambientales, sociales y culturales para prevenir la resistencia a los antibióticos, además de capacitar al personal de salud. Un enfoque ecosistémico es adecuado para alcanzar esta meta.
Palabras clave: Farmacorresistencia microbiana; agentes antibacterianos; prescripciones de medicamentos; población indígena; preescolar; estudios de intervención; Ecuador.
Infectious diseases remain the main cause of morbidity and mortality in low-and middle-income countries, especially among children in indigenous communities (1). In Ecuador, one of the poorest countries in Latin America, 22.5% of mortality among children < 1 year old was attributed in 2007 to pneumonia, bacterial sepsis, and diarrhea (2). While most of these conditions can be prevented with improved access to clean water, sanitation, personal hygiene, and immunization, use of antibiotics remains essential. Thus, preserving their efficacy is a global health priority (3).
Campaigns promoting careful use of antibiotics in highincome countries led to the conclusion that public campaigns can contribute to improved use of antibiotics in outpatients (46). However, little research has targeted low and middle-income countries, which not only bear the brunt of morbidity and mortality due to infectious disease but also face increasingly severe problems due to antibiotic resistance (7, 8). Factors contributing to antibiotic resistance in low and middle-income countries include lack of knowledge by health care professionals, deficient laboratory facilities, inadequate access to health care, lack of funds for appropriate antibiotic doses, dispensation of drugs by untrained people, and availability of substandard and counterfeit drugs (9). Transmission of resistant bacteria in low- and middle-income countries is facilitated by person-to-person contact through contaminated food and unsafe water. An understanding of this complex and multifactorial scenario is crucial to developing a containment strategy (9).
The ecosystem approach to human health recognizes the complexity of public health challenges and offers an alternative for addressing problems unresponsive to conventional strategies (10). Ecosystem approaches to health are "systemic, participatory approaches to understanding and promoting human health and well-being in the context of complex social and ecological interactions" (11). Recognizing that health is contingent on biophysical, social, economic, and political environments (justice and sustainability) necessitates transcending disciplines (transdisciplinarity), taking into account various perspectives (multistakeholder participation), and considering systemic inequities (social and gender equity) (12). An ecosystem approach to health, recently deemed to be one of the most important milestones in public health research (13), therefore seems ideally suited to this challenge.
This study, emerging within a 6-year project entitled "Sustainably Managing Environmental Health Risk in Ecuador," which embraces an ecosystem approach (14, 15), sought to ascertain whether applying an ecosystem approach with its principles of transdisciplinarity, equity, participation, and sustainability (13) could contribute to improving appropriate use of antibiotics and reducing the high prevalence of infectious disease.
In Cañar province, among the poorest in Ecuador, nearly 71.0% of the population is rural (16) and 80.0% of the people identify themselves as indigenous. Tucayta is an organization of farmer peasants spread across 15 settlements, including those in this study. Three students from these communities were recruited into the ecosystem master's program at the University of Cuenca, launched within this 6-year collaboration (14). With active participation of community members, these students conducted distinct but complementary thesis studies on water quality in the communities (17), reducing pesticide use (18), and preserving the water supply in the highlands to allow for clean water in the future (19). A dissertation of a doctoral student from Canada contributed to this knowledge base by improving understanding of how social capital can be harnessed in the community to reduce exposure to pesticides (20). A fourth master's student from the University of Cuenca (G.M.) focused her thesis on infectious diseases and antibiotic use (21).
Although all five theses inform an ecosystem approach to reducing the occurrence of infectious diseases, and their findings will be taken into account when planning a comprehensive multicomponent intervention, this article focuses on the findings of the latter study (21). The specific objectives were (a) to characterize areas such as environmental risk factors; knowledge, attitudes, and practices of caregivers; antibiotic use; and child health and (b) to seek community input in applying an ecosystem approach to the identified problems.
MATERIALS AND METHODS
This descriptive study was conducted to serve as a baseline assessment from which a longitudinal intervention study could be designed. It included a small pilot intervention to seek input from the community as to the elements to include in a longitudinal multicomponent ecohealth intervention trial.
Ecuador's national government operates the Fondo de Desarrollo Infantil program to provide childcare services and early stimulation for young children in the most vulnerable sectors of the Ecuadorian population. Virtually all children under age 5 years in these communities (98.0%) attend the program. All house-holds with children in the program who lived in the San José de La Posta and Correuco communities were included in this study, encompassing 65 households (31 in Correuco and 34 in La Posta) and 91 children (45 from Correuco and 46 from La Posta).
The following information was collected:
The household and infrastructure were characterized by using a rapid assessment procedure.
Each household's primary caregiver's knowledge, attitudes, and practices regarding infectious diseases and antibiotic use were collected with an internationally validated instrument (22). The knowledge, practices, and coverage survey was designed to provide a set of indicators of child health while promoting local participation in identifying health priorities and monitoring community health status (22). This study used modules from the survey on household, water and sanitation, breastfeeding and infant/ child nutrition, growth monitoring and child anthropometry, childhood immunization, diarrhea, and acute respiratory infection; modules were adapted to the cultural context of Ecuadorian communities and validated at Quilloac, another indigenous community near La Posta and Correuco.
Medicine chests were inspected.
The weight and height of all children < 5 years old were measured in order to determine nutritional status.
SPSS 13 was used for statistical analysis of collected data.
The protocol followed was approved by the joint CanadianEcuadorian University Partnered Ethics Committee, which oversaw these community-based research projects, as authorized by the National Council on Superior Education, the body that governs postgraduate education (resolution RCP.S06.No.258.05). The project was carefully explained at the beginning and signed informed consent was obtained from every caregiver (mother, father, grandparents).
The leaders of the Tucayta communities also provided informed consent for the authors to work in their communities. Every photograph taken during the research was taken after verbal consent was provided. A general consent form was obtained for the duration of the research project.
An ecohealth approach requires not only a systematic effort to incorporate community participation in decision making but also local understanding of etiology, as for community action research generally (23). (In order to have a comparison group against which to evaluate the effectiveness of an intervention at a future stage of the project, the community action/intervention component was conducted only in San José de La Posta, with Correuco left to serve as a comparison community.) After the topics were established, three community workshops were held that targeted caregivers. Content focused on the main issues identified in the risk factor analysis and household survey, with open dialogue and demonstrations about child health issues. The World Health Organization framework of driving forces, pressures, states, exposures, effects, and actions (DPSEEA) (24, 25)used by this team in other settingswas used to craft an ecosystem health intervention (26, 27).
Household and infrastructure
As shown in Table 1, households generally lacked sanitary services in both communities, especially for stool disposal. Only 32.3% of Correuco house-holds and 17.6% of La Posta households had a designated place for hand washing. In both communities, tap water was neither purified nor treated (67.7% and 82.7% in Correuco and La Posta, respectively), but only 9.7% of Correuco house-holds and 8.8% of La Posta households used bottled water. Hand washing was practiced before eating and before preparing foods in 20.0% to 30.0% of cases; only 19.0% of caregivers in Correuco and 8.8% in La Posta reported hand washing after changing diapers and after using the toilet.
Knowledge, attitudes, and practices
Breastfeeding and infant/child nutrition, growth monitoring and child anthropometry, childhood immunization.
Characteristics of the children are presented in Table 2. It is noteworthy that 26.3% and 29.2% of children in Correuco and La Posta, respectively, had not had complete immunizations. Although not shown in Table 2, it was noted that in the preceding 30 days, 31.9% of children had a diarrheic episode (26.7% in Correuco and 37% in La Posta); 28.9% of children from Correuco and 47.8% from La Posta incurred an acute respiratory tract infection; and, of them, 15.4% from Correuco and 50% from La Posta showed symptoms of respiratory distress. Regarding nutritional status, only 31% of children in Correuco and 13% in La Posta had adequate nutritional status as per the classification of Waterlow et al. for acute malnutrition (28).
Diarrhea and acute respiratory infection. As shown in Table 3, knowledge of medical treatment for diarrhea was correct as reported by only 29.0% and 17.6% of respondents from Correuco and La Posta, respectively. Knowledge of warning signs for diarrheal disease and acute respiratory tract infections was quite low.
Antibiotic use. As shown in Table 4, antibiotics were prescribed for more than 50% of cases of diarrhea; most commonly used was trimethoprim-sulfamethoxazole (40.0% in Correuco and 50.0% in La Posta), followed by amoxicillin in 20.0% of cases in Correuco. Antidiarrheal drugs for symptom relief were not used or prescribed. The results for respiratory tract infection were similar. As reported by caregivers, drugs were prescribed by doctors in most cases, but caregivers' responses to questions about dosage and treatment duration for diar-rheal disease and respiratory infections were incorrect in 100.0% of cases in Cor-reuco and 83.3% in La Posta; antibiotics for diarrhea were self-prescribed by a family member in 20.0% of cases in Cor-reuco; in La Posta, 33.3% of drugs for di-arrhea were prescribed at the pharmacy, which could be explained by the fact that two health centers are available to Cor-reuco's population but only one is close to La Posta. Only 80.0% of children in Correuco and 50.0% in La Posta finished their prescribed treatments for diarrhea; only 42.9% of cases of respiratory infection in Correuco and 54.5% in La Posta completed treatment as directed.
Medicine chest results
Antibiotics were present in 60.9% of households in Correuco and in 46.8% in La Posta (Figure 1).
Children's nutritional status
In both communities, there was a high rate of moderate (22.2% and 26.1% in Correuco and La Posta, respectively) and severe (6.7% and 6.5% in Correuco and La Posta, respectively) malnutrition.
Formulating the ecosystem approach
As shown in Table 5, application of the DPSEEA framework (21) identified that the health effects of greatest concern to the community were repeated diarrheic episodes and upper respiratory tract infections. With respect to exposures, it was noteworthy that piped water was found to be of poor quality by one member of the team, which, along with hygienic practices, perpetuates the cycle of agent exposure and infectious disease and seeking of medical treatment.
The state of the community was such that health personnel do not provide daily service in their community, and, according to community members who attended the workshop, often do not have updated knowledge; instead, they appear to rely on information provided by pharmaceutical companies. The community expressed the need for the health system to better consider Ecuador's ethnic and cultural diversity. In indigenous communities, the health of the ecosystem and that of humans are seen as one, with individual well-being linked to that of the community and the environment.
The driving forces and pressures component of Table 5 was derived by synthe-sizing the comments of the community and information gathered by other team members (1720) as well as other experts (29).
Those who participated in the meetings explicitly expressed appreciation in having obtained a baseline assessment of the communities for the purpose of designing an ecosystem approach to address these problems. A health party called "ally kawsay" (water, health, and joy) was thrown, encouraging the population to preserve their health.
Antimicrobial resistance is increasing worldwide, and it is a naturally occurring biological phenomenon; the process is amplified by use and misuse of antimicrobials (30). It is generally agreed that preventing the spread of resistance to existing and future antimicrobials requires using antimicrobials appropriately and reducing the burden of infectious disease through preventive hygiene and infection control practices (3133). Significant progress has been made in high-income countries through efforts such as characterizing knowledge, attitudes, and practices that determine prescribing (3437); training physicians in good prescribing practices (3739); having public education campaigns (4, 3741); and improving infection control (38). However, antibiotics in low- and middle-income countries are often available to the public from a variety of sources, including hospitals, pharmacies, licensed medicine stalls and drugstores, roadside stalls, and hawkers, as also found in this study. Moreover, this study found that geographic and cultural difficulties in accessing health care services result in a considerable proportion of the population seeking treatment at pharmacies, where personnel are not qualified to prescribe drugs.
In Correuco and San Jose de la Posta, although more than 90.0% of the population has tap water, its quality and safety are poor (19) with coliform bacteria present well above the permitted level. Unhygienic practices, such as inadequate water storage, untreated drinking water, and lack of hand washing, were very prevalent. Improving the quality of drinking water, education about hygienic practices, and access to sanitation are crucial to decreasing the burden of infectious disease and thus the need for antibiotics.
The findings in Correuco and La Posta enhance the notion that good-quality research is still lacking in the area of antimicrobial resistance, and integration of other important factors such as social, cultural, economic, and behavioral factors as well as the role of antimicrobials in agriculture and veterinary medicine needs to be taken into account when designing interventions. Further research on all the factors that influence antimicrobial use in these communities could provide a unique opportunity to gain knowledge about relevance to other indigenous and nonindigenous communities worldwide.
While this study achieved the objectives of providing a baseline description of many of the factors that might be driving the transmission of infectious diseases as well as inappropriate antibiotic use, its limitations include the fact that not all environmental factors could be rigorously evaluated. Also antibiotic use was characterized only from a survey of caregivers; further research involving health providers and pharmacists is desirable. Child health was also evaluated only from a symptom survey and clinical examination conducted by the lead author; reviews of medical records might provide a deeper understanding of the incidence and prevalence of infectious diseases and appropriate use of antibiotics.
It is clear that the knowledge, attitudes, and practices of caregivers, although undoubtedly relevant, fall short of explaining the magnitude of the problem. Child malnutrition, poor water quality, and lack of proper sanitation combined with other social and environmental factors must be taken into consideration. Now that the baseline assessment has been conducted and community interest was piqued, the stage is set for formulating and rigorously evaluating a comprehensive ecosystem approach to this important health problem.
The authors thank their colleagues from Ecuador and Canada as well as the community of Tucayta and especially the caregivers who contributed to this study with their knowledge, active participation, and commitment to raise their children in the best possible context. This paper originated as Georgina
Muñoz's master's thesis in the Ecosystem Approach to Health program at the University of Cuenca. This master's program was part of a larger project launched in 2004 on sustainably managing environmental health risk in Ecuador involving Canadian, Cuban, and Mexican partners and four Ecuadorian universities with funding from the Canadian International Development Agency.
1. World Health Organization. WHO global burden of disease: 2004 update. Geneva: WHO; 2008. [ Links ]
2. Ministerio de Salud Pública del Ecuador. Indicadores básicos de salud. Ecuador 2008. Quito: Ministerio de Salud Pública del Ecuador; 2008. Available from: http://new.paho.org/ecu/index.php?option=com_content& task=view&id=25&Itemid=135 Accessed 12 December 2010. [ Links ]
3. Choffnes E. Antibiotic resistance: implications for global health and novel intervention strategies: workshop. Washington, D.C.: National Academies Press; 2010. [ Links ]
4. Huttner B, Goossens H, Verheij T, Harbarth S, on behalf of the CHAMP consortium. Characteristics and outcomes of public campaigns aimed at improving the use of antibiotics in outpatients in high-income countries. Lancet Infect Dis. 2010;10:1731. [ Links ]
5. Ranji SR, Steinman MA, Shojania KG, Gonzales R. Interventions to reduce unnecessary antibiotic prescribing: a systematic review and quantitative analysis. Med Care. 2008;46(8):84762. [ Links ]
6. Finch RG, Metlay JP, Davey PG, Baker LJ. Educational interventions to improve antibiotic use in the community: report from the International Forum on Antibiotic Resistance (IFAR) colloquium, 2002. Lancet Infect Dis. 2004;4(1):4453. [ Links ]
7. Okeke I, Fayinka S, Lamikanra A. Antibiotic resistance in Escherichia coli from Nigerian students, 19861998. Emerg Infect Dis. 2000;6:3936. [ Links ]
8. Zhang R, Eggleston K, Rotimi V, Zeckhauser RJ. Antibiotic resistance as a global threat: evidence from China, Kuwait and the United States. Global Health. 2006;2:6. [ Links ]
9. Bartoloni A, Gotuzzo E. Bacterial-resistant infections in resource-limited countries In: Sosa AdJ, Byarugaba DK, Amábile-Cuevas CF, Hsueh PR, Kariuk S, Okeke IN, eds. Antimicrobial resistance in developing countries. New York: Springer; 2010. Pp. 199231. [ Links ]
10. Aryaa N. Time for an ecosystem approach to public health? Lessons from two infectious disease outbreaks in Canada. Global Public Health. 2009;4(1):3149. [ Links ]
11. Waltner-Toews D. Food, global environmental change and health: EcoHealth to the rescue? McGill Med J. 2009;12(1):859. [ Links ]
12. Lebel J. Health: an ecosystem approach. Ottawa: International Development Research Centre; 2003. [ Links ]
13. Webb J, Mergler D, Parkes M, Saint-Charles J, Spiegel J, Waltner-Toews D, et al. Tools for thoughtful action: the role of ecosystem approaches to health in enhancing public health. Can J Public Health. 2010;101(6):43941. [ Links ]
14. Parkes M, Spiegel J, Breilh J, Cabarcas F, Huish R, Yassi A. Building sustainable capacity to promote the health of marginalized populations through international collaboration: examining community-oriented training innovations in Ecuador. Bull World Health Organ. 2009;87(4):245324. [ Links ]
15. Spiegel J, Breilh J, Beltran E, Parra J, Solis F, Yassi A, et al. Establishing a community of practice of researchers, practitioners, policy-makers and communities to sustainably manage environmental health risks in Ecuador. BMC Intern Health Hum Rights. 2011;11(Suppl 2):S25. [ Links ]
16. Instituto Nacional de Estadísticas y Censos. Consejo provincial del Cañar. Azogues, Cañar, Ecuador: Instituto Nacional de Estadísticas y Censos; 2001. Available from: http://www.hcpcanargov.ec/hcpc_ccanar.asp Accessed 6 December 2010. [ Links ]
17. Guaman C. Evaluation of contaminated water from Cañar City, its impact on the population and its mitigation through community participation. Tucayta, Cuenca, Ecuador: University of Cuenca; 2009. [ Links ]
18. Alulema R. Pesticide contamination of Andean production systems of Quilloac and San Rafael communities TucaytaCañar. Cuenca, Ecuador: University of Cuenca; 2008. [ Links ]
19. Verdugo M. Sustainable participatory management of the highlands of Patococha Tucayta, Cañar. Cuenca, Ecuador: University of Cuenca; 2008. [ Links ]
20. Cabarcas F. Harnessing the community capacity of small farmer organizations to reduce pesticide-related environmental health risks: a case study in an indigenous community in the southern ranges of Ecuador. Vancouver, British Columbia, Canada: University of British Columbia; 2010. [ Links ]
21. Muñoz G. Infectious diseases and antibiotic use among children under 5 years from Tucayta's organization indigenous communities of Correuco and La Posta. Cuenca, Ecuador: University of Cuenca; 2008. [ Links ]
22. Edison J, Child Survival Technical Support Project, CORE Monitoring and Evaluation Working Group. KPC 2000+: knowledge, practices and coverage survey: tools and field guide. Calverton, Maryland: Child Survival Technical Support Group; 2000. [ Links ]
23. Wallerstein NB, Duran B. Using community-based participatory research to address health disparities. Health Promot Pract. 2006;7(3):31223. [ Links ]
24. Corvalán CF, Kjellström T, Smith KR. Health, environment and sustainable development: identifying links and indicators to promote action. Epidemiology. 1999;10:65660. [ Links ]
25. Dannenberg A, Frumkin H, Jackson RJ. Making healthy places: a built environment for health, well-being, and sustainability. Washington, D.C.: Island Press; 2011. [ Links ]
26. Spiegel JM, Bonet M, Tate GM, Ibarra AM, Tate B, Yassi A. Building capacity in central Havana to sustainably manage environmental health risk in an urban ecosystem. EcoHealth J. 2004;1(Suppl. 2):12030. [ Links ]
27. Spiegel JM, Bonet M, Yassi A, Tate R, Concepción M, Cañizares M. Evaluating the effectiveness of a multicomponent intervention to improve health in an inner city Havana community. Int J Occup Environ Health. 2003;9(2):11827. [ Links ]
28. Waterlow JC, Buzina R, Keller W, Lane JM, Nichaman MZ, Tanner JM. The presentation and use of height and weight data for comparing the nutritional status of groups of children under the age of 10 years. Bull World Health Organ. 1977;55(4):48998. [ Links ]
29. Perafán CW. Los pueblos indígenas y la salud: cuestiones para la discusión y el debate. Washington, D.C.: Banco Interamericano de Desarrollo; 2001. [ Links ]
30. Sirinavin S, Dowell SF. Antimicrobial resistance in countries with limited resources: unique challenges and limited alternatives. Semin Pediatr Infect Dis. 2004;15(2):948. [ Links ]
31. International Conference on Improving Use of Medicines. Theme summary: antimicrobial resistance. Washington, D.C.: International Conference on Improving Use of Medicines; 2004. [ Links ]
32. International Conference on Improving Use of Medicines. Policies and programs to improve use of medicines: recommendations from ICIUM 2004. Washington, D.C.: International Conference on Improving Use of Medicines; 2004. [ Links ]
33. Weinstein RA. Controlling antimicrobial resistance in hospitals: infection control and use of antibiotics. Emerg Infect Dis. 2001;7(2): 18892. [ Links ]
34. Macfarlane J, Holmes W, Macfarlane R, Britten N. Influence of patients' expectations on antibiotic management of acute lower respiratory tract illness in general practice: questionnaire study. BMJ. 1997;315(7117):12114. [ Links ]
35. Butler CC, Rollnick S, Pill R, Maggs-Rapport F, Stott N. Understanding the culture of prescribing: qualitative study of general practitioners' and patients' perceptions of antibiotics for sore throats. BMJ. 1998;317(7159):63742. [ Links ]
36. Bauchner H. Parents' impact on antibiotic use. APUA Newsletter. 1997;15(2):13. [ Links ]
37. McKay R, Vrbova L, Fuertes E, Chong M, David S, Dreher K, et al. Evaluation of the Do Bugs Need Drugs? program in British Columbia: can we curb antibiotic prescribing? Can J Infect Dis. 2011;22(1):1924. [ Links ]
38. Jindrak V, Marek J, Vanis V, Urbaskova P, Vlcek J, Janiga L, et al. Improvements in antibiotic prescribing by community paedia-tricians in the Czech Republic. Euro Surveill. 2008;13(46):46. [ Links ]
39. Mölstad S, Erntell M, Hanberger H, Melander E, Norman C, Skoog G, et al. Sustained reduction of antibiotic use and low bacterial resistance: 10-year follow-up of the Swedish Strama programme. Lancet Infect Dis. 2008;8(2):12532. [ Links ]
40. Goossens H, Coenen S, Costers M, De Corte S, De Sutter A, Gordts B, et al. Achievements of the Belgian Antibiotic Policy Coordination Committee (BAPCOC). Euro Surveill. 2008;13:46. [ Links ]
41. Prins JM, Degener JE, de Neeling AJ, Gyssens IC, SWAB Board. Experiences with the Dutch Working Party on antibiotic policy (SWAB). Euro Surveill. 2008;13:46. [ Links ]
Manuscript received on 8 April 2011. Revised version accepted for publication on 31 October 2011.