Using a pharmacist-led educational tool to teach elementary and middle-school students in Lebanon about microbes, antibiotic use and antimicrobial resistance: A pilot study
DOI:
https://doi.org/10.46542/pe.2023.231.4760Keywords:
Antibiotics, Antimicrobial resistance, School, Pharmacist-led educationAbstract
Background: Teaching school students about antibiotic use and antimicrobial resistance (AMR) can shape their future behaviour to become antibiotic guardians. This study aims to assess the impact of a pharmacist-led educational tool in boosting knowledge of these topics at elementary and middle school educational stages.
Methods: A prospective web-based cross-sectional pre-post study was conducted in Lebanese private schools from April 2020 to December 2021.
Results: The results showed that the pharmacist-led intervention increased the general knowledge (p = 0.01) and understanding of microbes (junior versus senior, p = 0.003 versus p = 0.004). In middle school, the spread of infection (p < 0.001) and the AMR concept (p = 0.001) significantly changed post-test, while antibiotics use and AMR concept remained unchanged in elementary students.
Conclusion: The successful learning impact of the educational tool designed and led by pharmacists shows their importance as antibiotic experts in influencing early pedagogic learning about antibiotics and AMR starting at the middle-school stage.
References
Ambusaidi, A., Taylor, N., Quinn, F., Rizk, N., & Taylor, S. (2022). Omani senior secondary school students’ knowledge of and attitudes to antibiotic resistance. PloS one, 17(2)
Antunes, P., Novais, C., Novais, Â., Grosso, F., Ribeiro, T. G., Mourão, J., Perovic, S.U., Rebelo, A., Ksiezarek, M., Freitas, A.R. & Peixe, L. (2021). MicroMundo@ UPorto: an experimental microbiology project fostering student's antimicrobial resistance awareness and personal and social development. FEMS Microbiology Letters, 368(4). https://doi.org/10.1093/femsle/fnab016
Appiah, B., Asamoah-Akuoko, L., Samman, E., Koduah, A., Kretchy, I.A., Ludu, J. Y., Odonkor, G., Nam, S.H., & Gyansa-Luterrodt, M. (2022). The impact of antimicrobial resistance awareness interventions involving schoolchildren, development of an animation and parents engagements: a pilot study. Antimicrobial resistance and infection control, 11(1), 26. https://doi.org/10.1186/s13756-022-01062-6
Azevedo, M.M., Pinheiro, C., Yaphe, J., & Baltazar, F. (2009). Portuguese students' knowledge of antibiotics: a cross-sectional study of secondary school and university students in Braga. BMC Public Health, 9(1), 1-6
Azevedo, M.M., Pinheiro, C., Yaphe, J., & Baltazar, F. (2013). Assessing the impact of a school intervention to promote students’ knowledge and practices on correct antibiotic use. International Journal of Environmental Research and Public Health, 10(7), 2920-2931
Balasegaram, M., Pécoul, B., Gray, G., Sharland, M., & Swaminathan, S. (2019). Hard to study, hard to treat: putting children at the centre of antibiotic research and development. Lancet. Infectious Diseases, 19(6), 573-574
Barua, A., Kademane, K., Gubbiyappa, K.S., Verma, R.K., Iqbal, M.S., & Al-Dubai, S.A.R. (2013). A tool for decision-making in norm-referenced survey questionnaires with items of continuous variables. Journal of Asian Scientific Research, 3(11), 1109-1118
Brito Avô, A., Costa, C., Amann, G., Gaspar, M.J., & Batista, I. (2011). Implementation of the e-Bug Project in Portugal. Journal of antimicrobial chemotherapy, 66(suppl_5), v81-v83
Cassini, A., Högberg, L.D., Plachouras, D., Quattrocchi, A., Hoxha, A., Simonsen, G.S., Colomb-Cotinat, M., Kretzschmar, M.E., Devleesschauwer, B., Cecchini, M., Ouakrim, D.A., Oliveira, T.C., Struelens, M.J., Suetens, C., Monnet, D.L. & Hopkins, S. (2019). Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. The Lancet infectious diseases, 19(1), 56-66
Cebotarenco, N., & Bush, P.J. (2008). Reducing antibiotics for colds and flu: a student-taught program. Health education research, 23(1), 146-157
Daoud, Z. (2018). Antimicrobial Resistance in the One Health Concept in Lebanon. Journal of Infection in Developing Countries, 12(2), 2S
Dassner, A. M., Nicolau, D. P., & Girotto, J. E. (2017). Management of Pneumonia in the Pediatric Critical Care Unit: An Area for Antimicrobial Stewardship. Current pediatric reviews, 13(1), 49–66. https://doi.org/10.2174/1573396312666161205102221
De Castro, P., Barbaro, M.C., Salinetti, S., Carinci, A., Pantosti, A., Lecky, D.M., Hawking, M.K.D., & McNulty, C.A. (2013). Information and health literacy for school students: the e-Bug experience in Italy. Journal of the European Association for Health Information and Libraries, 9(1), 8
Eveillard, M., Ruvoen, N., Lepelletier, D., Fradet, S., Couvreur, S., Krempf, M., & Magras, C. (2016). Integration of microbiology and infectious disease teaching courses in an interdisciplinary training programme (Master level) centred on the ‘One world, one health’ WHO concept. FEMS Microbiology Letters, 363(9), fnw068
Farrell, D., Kostkova, P., Lazareck, L., Weerasinghe, D., Weinberg, J., Lecky, D.M., Adraenssens, N., Herotova, T.K., Holt, J., Touboul, P., Merakou, K., Koncan, R., Olczak-Pienkowska, A., Avo, A.B., Campos, J., & McNulty, C.A.M. (2011). Developing e-Bug web games to teach microbiology. Journal of Antimicrobial Chemotherapy, 66(suppl_5), v33-v38. https://doi.org/10.1093/jac/dkr121
Fernandes, R., Naik, S., Bhat, A. G., Shetty, R., Hande, M. H., Ghafur, A., Rao, M., Kunhikatta, V., & Pathiraj, J. P. (2019). Knowledge Assessment of E-Bug Assisted Antimicrobial Resistance Education Module in Class VII School Students of South Indian Coastal Town of Manipal. Journal of clinical medicine, 8(1), 84. https://doi.org/10.3390/jcm8010084
Fletcher-Miles, H., Gammon, J., Williams, S., & Hunt, J. (2020). A scoping review to assess the impact of public education campaigns to affect behavior change pertaining to antimicrobial resistance. American Journal of Infection Control, 48(4), 433-442
Fonseca, M.J., Santos, C.L., Costa, P., Lencastre, L., & Tavares, F. (2012). Increasing awareness about antibiotic use and resistance: a hands-on project for high school students. PloS one, 7(9). https://doi.org/10.1371/journal.pone.0044699
Gawai, P.P., Taware, S.A., Chatterjee, A.S., & Thakur, H.P. (2016). A cross sectional descriptive study of hand washing knowledge and practices among primary school children in Mumbai, Maharashtra, India. International Journal of Community Medicine and Public Health, 3(10), 2958-2966
Gennimata, D., Merakou, K., Barbouni, A., & Kremastinou, J. (2011). Implementation of the e-Bug Project in Greece. Journal of Antimicrobial Chemotherapy, 66(suppl_5), v71-v73
Hayes, C., Young, V., Brown, C., Touboul Lundgren, P., Gennimata, D., Holt, J., Weisheit, E., Rico, A., Garcia, C., De Castro, P., & McNulty, C.A.M. (2020). International promotion of e-Bug, an infection prevention and control educational intervention: survey of partners across 14 countries. JAC-antimicrobial resistance, 2(1). https://doi.org/10.1093/jacamr/dlaa003
Henaine, A.M., Lahoud, N., Abdo, R., Shdeed, R., Safwan, J., Akel, M., Fahs, I., Zeenny, R., Sacre, H., Hallit, S., & Salameh, P. (2021). Knowledge of Antibiotics Use among Lebanese Adults: A study on the influence of sociodemographic characteristics. Sultan Qaboos University medical journal, 21(3), 442–449. https://doi.org/10.18295/squmj.4.2021.006
Holt, J., & Jensen, U.S. (2011). Implementation of e-Bug in Denmark. Journal of antimicrobial chemotherapy, 66(suppl_5), v59-v62
Hsia, Y., Sharland, M., Jackson, C., Wong, I.C., Magrini, N., & Bielicki, J.A. (2019). Consumption of oral antibiotic formulations for young children according to the WHO Access, Watch, Reserve (AWaRe) antibiotic groups: an analysis of sales data from 70 middle-income and high-income countries. The Lancet Infectious Diseases, 19(1), 67-75
Kvint, K., Palm, M., & Farewell, A. (2020). Teaching about antibiotic resistance to a broad audience: A multidisciplinary approach. FEMS microbiology letters, 367(14), fnaa111
Laxminarayan, R., & Bhutta, Z.A. (2016). Antimicrobial resistance—a threat to neonate survival. The Lancet Global Health, 4(10), e676-e677
Lecky, D.M., McNulty, C.A., Adriaenssens, N., Herotová, T.K., Holt, J., Kostkova, P., Merakou, K., Koncan, R., Olczak-Pienkowska, A., Avo, A.B., Campos, J., Farrel, D., Touboul, P., Barbouni, N., Benes, J., Caballero, C.R., Cornaglia, G., De Corte, S., de Quincey, E., Dellamonica, P., Gennimata, D., Goossens, H., Grzesiowski, P., Kremastinou, J., Noer, M., & Weinberg, J. (2011). Development of an educational resource on microbes, hygiene and prudent antibiotic use for junior and senior school children. Journal of Antimicrobial Chemotherapy, 66(suppl_5), v23-v31
Lecky, D.M., McNulty, C.A., Touboul, P., Herotova, T.K., Benes, J., Dellamonica, P., Verlander, N.Q., Kostkova, P., Weinberg, J., & e-Bug Working Group (2010). Evaluation of e-Bug, an educational pack, teaching about prudent antibiotic use and hygiene, in the Czech Republic, France and England. The Journal of Antimicrobial Chemotherapy, 65(12), 2674–2684. https://doi.org/10.1093/jac/dkq356
Lee, C.R., Lee, J.H., Kang, L.W., Jeong, B.C., & Lee, S.H. (2015). Educational effectiveness, target, and content for prudent antibiotic use. BioMed research international, 2015, 214021. https://doi.org/10.1155/2015/214021
Leung, A.K., Wong, A.H., Leung, A.A., & Hon, K.L. (2019). Urinary tract infection in children. Recent patents on inflammation & allergy drug discovery, 13(1), 2-18
Little, P., Stuart, B., Hobbs, F.D., Moore, M., Barnett, J., Popoola, D., Middleton, K., Kelly, J., Mullee, M., Raftery, J., Yao, G., Carman, W., Fleming, D., Stokes-Lampard, H., Williamson, I., Joseph, J., Miller, S., & Yardley, L. (2015). An internet-delivered handwashing intervention to modify influenza-like illness and respiratory infection transmission (PRIMIT): a primary care randomised trial. Lancet, 386(10004), 1631–1639. https://doi.org/10.1016/S0140-6736(15)60127-1
McParland, J.L., Williams, L., Gozdzielewska, L., Young, M., Smith, F., MacDonald, J., Langdridge, D., Davis, M., Price, L., & Flowers, P. (2018). What are the 'active ingredients' of interventions targeting the public's engagement with antimicrobial resistance and how might they work?. British journal of health psychology, 23(4), 804–819. https://doi.org/10.1111/bjhp.12317
Mouhieddine, T.H., Olleik, Z., Itani, M.M., Kawtharani, S., Nassar, H., Hassoun, R., Houmani, Z., El Zein, Z., Fakih, R., Mortada, I.K., Mohsen, Y., Kanafani, Z., & Tamim, H. (2015). Assessing the Lebanese population for their knowledge, attitudes and practices of antibiotic usage. Journal of infection and public health, 8(1), 20–31. https://doi.org/10.1016/j.jiph.2014.07.010
Murray, C.J., Ikuta, K.S., Sharara, F., Swetschinski, L., Aguilar, G.R., Gray, A., Han, C., Bisignano, C., Rao, P., Wool, E., Johnson, S.C., Browne, A.J., Chipeta, M.C., Fell, F., Hackett, S., Haines-Woodhouse, G., Hamadani, B.H.K., Kumaran, E.A.P., McManigal, B., Achalapong, S., Agarwal, R., Akech, S., Albertson, S., Amuasi, J., Andrews, J., Aravkin, A., Ashley, E., Babin, F-.X., Bailey, F., Baker, S., Basnyat, B., Bekker, A., Bender, R., Berkley, J.A., Bethou, A., Bielicki, J., Boonkasidecha, S., Bukosia, J., Carvalheiro, C., Castañeda-Orjuela, C., Chansamouth, V., Chaurasia, S., Chiurchiù, S., Chowdhury, F., Donatien, R.C., Cook, A.J., Cooper, B., Cressey, T.R., Criollo-Mora, E., Cunningham, M., Darboe, S., Day, N.P.J., De Luca, M., Dokova, K., Dramowski, A., Dunachie, S.J., Bich, T.D., Eckmanns, T., Eibach, D., Emami, A., Feasey, N., Fisher-Pearson, N., Forrest, K., Garcia, C., Garrett, D., Gastmeier, P., Giref, A.Z., Greer, R.C., Gupta, V., Haller, S., Haselbeck, A., Hay, S.I., Holm, M., Hopkins, S., Hsia, Y., Iregbu, K.C., Jacobs, J., Jarovsky, D., Javanmardi, F., Jenney, A.W.J., Khorana, M., Kissoon, N., Kobeissi, E., Kostyanev, T., Phommasone, K., Khusuwan, S., Krapp, F., Krumkamp, R., Kumar, A., Kyu, H.H., Lim, C., Lim, K., Limmathurotsakul, D., Loftus, M.J., Lunn, M., Ma, J., Manoharan, A., Marks, F., May, J., Mayxay, M., Mturi, N., Munera-Huertas, T., Musicha, P., Musila, L.A., Mussi-Pinhata, M.M., Naidu, R.N., Nakamura, T., Nanavati, R., Nangia, S., Newton, P., Ngoun, C., Novotney, A., Nwakanma, D., Obiero, C.W., Ochoa, T.J., Olivas-Martinez, A., Olliaro, P., Ooko, E., Ortiz-Brizuela, E., Ounchanum, P., Pak, G.D., Paredes, J.P., Peleg, A.Y., Perrone, C., Phe, T., Plakkal, N., Ponce-de-Leon, A., Raad, M., Ramdin, T., Rattanavong, S., Riddell, A., Roberts, T., Robotham, J.V., Roca, A., Rosenthal, V.D., Rudd, K.E., Russell, N., Sader, H.S., Saengchan, W., Schnall, J., Scott, J.A.G., Seekaew, S., Sharland, M., Shivamallappa, M., Sifuentes-Osornio, J., Steenkeste, A.J.S.N., Stewardson, A.J., Stoeva, T., Tasak, N., Thaiprakong, A., Thwaites, G., Tigoi, C., Turner, C., Turner, P., van Doorn, H.R., Velaphi, S., Vongpradith, A., Vongsouvath, M., Vu, H., Walsh, T., Walson, J.L., Waner, S., Wangrangsimakul, T., Wannapinij, P., Wozniak, T., Young-Sharma, T.E.M.W., Yu, K.C., Zheng, P., Sartorius, B., Lopez, A.D., Stergachis, A., Moore, C., Dolecek, C. & Naghavi, M. (2022). Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. The Lancet, 399(10325), 629-655
Osman, M., Kasir, D., Kassem, I.I., & Hamze, M. (2021). Shortage of appropriate diagnostics for antimicrobial resistance in Lebanese clinical settings: a crisis amplified by COVID-19 and economic collapse. Journal of Global Antimicrobial Resistance, 27, 72
Rodríguez, C., González, E., García, A., & Campos, J. (2011). Implementation of the e-Bug Project in Spain. Journal of antimicrobial chemotherapy, 66(suppl_5), v85-v87
Sakr, S., Ghaddar, A., Hamam, B., & Sheet, I. (2020). Antibiotic use and resistance: An unprecedented assessment of university students’ knowledge, attitude and practices (KAP) in Lebanon. BMC Public Health, 20(1), 1-9
Taylor, J.A., Kwan-Gett, T.S.C., & McMahon Jr, E.M. (2003). Effectiveness of an educational intervention in modifying parental attitudes about antibiotic usage in children. Pediatrics, 111(5), e548-e554
Touboul, P., Dunais, B., Urcun, J.M., Michard, J.L., Loarer, C., Azanowsky, J.M., Vincent, I., Jestin, C., Housseau, B., de Warren, A. & Dellamonica, P. (2011). The e-Bug project in France. Journal of antimicrobial chemotherapy, 66(suppl_5), v67-v70
Valderrama, M.J., González-Zorn, B., de Pablo, P.C., Díez-Orejas, R., Fernández-Acero, T., Gil-Serna, J., de Juan, L., Martin, H., Molina, M., Navarro-Garcia, F., Patino, B., Pla, J., Prieto, D., Rodriguez, C., Roan, E., Sanz-Santamaria, A.B., de Siloniz, M.I., Suarez, M., Vazquez, C., & Cid, V.J. (2018). Educating in antimicrobial resistance awareness: adaptation of the Small World Initiative program to service-learning. FEMS microbiology letters, 365(17), fny161. https://doi.org/10.1093/femsle/fny161
WHO (World Health Organisation). (2021) Antimicrobial resistance. Available from: https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance
Young, V. L., Cole, A., Lecky, D. M., Fettis, D., Pritchard, B., Verlander, N. Q., Eley, C. V., & McNulty, C. A. M. (2017). A mixed-method evaluation of peer-education workshops for school-aged children to teach about antibiotics, microbes and hygiene. The Journal of antimicrobial chemotherapy, 72(7), 2119–2126. https://doi.org/10.1093/jac/dkx083
Zhang, Y., Kabba, J., Chang, J., Ji, W., Zhu, S., Yu, J., Xu, S., & Fang, Y. (2018). A School-Based Educational Intervention for School-Aged Children and Caregivers about Rational Use of Antibiotics in Urban Areas of Shaanxi Province: A Study Protocol for a Randomized Controlled Research.International journal of environmental research and public health, 15(9), 1912. https://doi.org/10.3390/ijerph15091912