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Background Antimicrobial resistance (AMR) is a global health security threat and is associated with increased mor- bidity and mortality. One of the key drivers of AMR is the inappropriate use of antibiotics. A key component of improv- ing antibiotic use is conducting antimicrobial use (AMU) surveillance. Methods USAID Medicines Technologies and Pharmaceutical Services Program has supported the implementation of antimicrobial stewardship activities, including setting up systems for AMU surveillance in Tanzania and Uganda. Results from both countries have been previously published. However, additional implementation experience and les- sons learned from addressing challenges to AMU surveillance have not been previously published and are the subject of this narrative article. Results The team identified challenges including poor quality data, low digitalization of tools, and inadequate resources including both financial and human resources. To address these gaps, the Program has supported the use of continuous quality improvement approaches addressing gaps in skills, providing tools, and developing guidelines to fill policy gaps in AMU surveillance. Recommendations to fill these gaps, based on the Potter and Brough system- atic capacity building model have been proposed. Conclusions Strengthening AMU surveillance through using a capacity-building approach will fill gaps and strengthen efforts for AMR control in both countries. Keywords Antimicrobial resistance, Antimicrobial use surveillance, Capacity building, Health system, Africa, Global health security, Point prevalence survey, Tanzania, Uganda *Correspondence: Reuben Kiggundu firstname.lastname@example.org Full list of author information is available at the end of the article © The Author(s) 2023. 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The Creative Commons Public Domain Dedication waiver (http://creativecom- mons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Kiggundu et al. Antimicrobial Resistance & Infection Control (2023) 12:9 Page 2 of 8 countries. In Tanzania and Uganda, the Program works Background with in-country entities such as the Ministry of Health, Antimicrobial resistance (AMR) is a sustainable devel- the Multisectoral Coordinating Committee and Tech- opment challenge and global health security threat. It nical Working Groups (TWG), health facilities, pro- threatens progress toward several sustainable devel- fessional and regulatory bodies, academic institutions opment goals including health. [1, 2]. In 2019, AMR such as Muhimbili University of Allied and Health Sci- was estimated to directly cause an estimated 1.27mil- ences and Catholic University of Allied and Health Sci- lion deaths, with a further 4.95 indirect deaths  AMR ences in Tanzania, Makerere University in Uganda, and threatens global development initiatives including efforts the University of Washington as a global learning part- to control infectious diseases . Multiple efforts to ner. The Program uses a multi-pronged capacity building control AMR are currently ongoing [4–7], including the approach through training, provision of tools and guide- Global Action Plan which proposes 5 strategic objectives, lines, on-site mentorship, and supportive supervision at including optimizing the use of antimicrobial agents . the health facility level. The Program works in 10 and 13 Antimicrobial Use Surveillance (AMU) is a component of hospitals Tanzania and Uganda, respectively and AMU the optimization of the use of antimicrobial agents. surveillance findings from these were recently published Inappropriate use of antibiotics is a major driver of [16, 17]. More work on AMU surveillance from both AMR and can be observed in many forms but not limited countries has also been published [18–20]. to: wrong dose, wrong indication, incomplete dosage, Despite these efforts, gaps in implementing and sus - inappropriate prescribing, and poor disposal of medi- taining AMU surveillance remain. In this context, based cal waste . It is therefore imperative that we develop on our experiences, we describe current challenges and systems for AMU . In addition to understanding how propose recommendations for improving AMU surveil- antibiotics are used, AMU surveillance can inform the lance in Tanzania and Uganda and by extension could be implementation of the WHO Access, Watch, and Reserve used by other LMICs. (AWaRe)  categorization of antibiotics and the WHO Global Antimicrobial Resistance Surveillance System Challenges facing AMU surveillance in Tanzania (GLASS) . and Uganda The WHO’s International Health Regulations (IHR) Although efforts to strengthen AMU surveillance are Benchmark 3.4 on optimizing use of antimicrobials ongoing, challenges remain as described below. recommended that member states monitor antimicro- bial use, among other antimicrobial stewardship (AMS) Inadequate data systems including sub‑optimal data activities, in designated health facilities to reach level 3 sources and low digitalization (“developed capacity”) with progression to level 4 (“dem- The capacity to collect and report high-quality data is onstrated capacity”) and finally to level 5 (“sustainable crucial for successful AMU surveillance. First, in both capacity”) . A recent WHO report found that most countries, ineligible handwriting, missing patient files, low and middle-income countries (LMICs) did not have incomplete medical records, e.g., lack of diagnosis or pre- systems for AMU surveillance . In several countries, scription notes were a challenge during data collection. available data is fragmented or available as “snapshot” Second, although Health Management Information Sys- research. Thus there is no comprehensive reflection tem (HMIS) tools are available in both countries, AMU of AMU surveillance and factors that influence it , surveillance data collection indicators have not been inte- hence the need for capacity building in this area. grated into these tools, hence the need for introduction of revised tools. This negatively affects the interoperabil - The context ity of data systems and leads to additional strain on the The Medicines, Technologies and Pharmaceutical Ser - available resources. In both countries, the AMU tool and vices Program (henceforth called “the Program”) is a five- data sources were manual which increased the level of year Program led by Management Sciences for Health effort and raised the risks of error during data extraction. and funded by the United States Agency for Interna- Third, there is limited use of standard coding of disease tional Development . The Program uses a One Health in both countries, with wide variation in nomenclature approach to build AMR control capacities in 13 LMICs. of diagnosis. For example, while some clinicians wrote Our work focuses on strengthening multisectoral col- the diagnosis as lower respiratory tract infection, others laboration, infection prevention and control and AMS wrote pneumonia. Another common cause of discrep- and is guided by a country’s AMR National Action Plan ancy was urinary tract infection versus the use of other (NAP) and WHO Benchmarks for IHR . Under AMS, terminologies like pyelonephritis or cystitis. This cre - the Program is building systems for AMU surveillance ated discrepancy in the indication for use of antibiotics through provision of technical assistance to selected K iggundu et al. Antimicrobial Resistance & Infection Control (2023) 12:9 Page 3 of 8 both within hospitals, between hospitals and between On the other hand, classification of antibiotics required countries. Lastly, antibiotic prescriptions obtained from a pharmacy technician or pharmacist. The Program outside the hospital dispensing systems could not be ver- set up multidisciplinary teams, supported by our staff, ified since prescriptions were not available in the hospi - national level experts and facility-based health work- tal records. With a high stockout of essential medicines ers to conduct the AMU surveillance, overcoming these in LMICs, improving data management for medicines challenges in the process. Most hospitals did not have the obtained outside the hospital pharmacy system is essen- technical expertise to constitute a multidisciplinary team tial to understanding hospital antibiotic use pathways with experience in AMU surveillance. As such, the Pro- . gram provided technical expertise for the activity, with input from in-country academic institutions, Ministries Lack of appropriate tools for AMU surveillance of Health, and individual consultants. The University of As highlighted from AMU surveillance reports published Washington provided data analysis and data manage- from both countries, there is variability of methodolo- ment support for the Uganda AMU surveillance. Another gies [18, 20, 22]. However, the Program’s experience is observation was the absence of adequate structures for based on the use of the WHO Point Prevalence Survey AMS in the health facilities. Since AMU surveillance is methodology . Although the tool has been developed a component of AMS, it is critical that systems for AMS in the context of LMICs, data on some of the variables are present in participating hospitals. The Program is was not readily available in the medical record system of working to address this gap. both countries. For example, data on whether the patient is having a nasogastric tube or urinary catheter is not Limited financing for AMU surveillance at all levels normally captured in patient files and the data collec - AMU surveillance activities are often not routinely tors had to examine patients to confirm if or not patients funded through hospital budgets nor through a formal had these in place. Similarly, data on other patient vari- budget line item in Ministries of Health. Consequently, ables like human immunodeficiency virus status, tuber - the program fully funded the activities. Table 1 summa- culosis, antiretroviral therapy, CD4 count, McCabe score rizes the costs of the AMU surveillance in both coun- and, malnutrition status is not collected in a standard tries. We intentionally share the costs knowing that it way, with physician preference and practices determin- is not found in the literature. Tanzania is almost four ing if this data is collected and recorded in the patient times the geographical size of Uganda and our interven- chart as part of the clinical notes. To avoid missing tion hospitals in Tanzania are geographically dispersed data, the research assistants had to search for additional across regions compared to Uganda. We found the costs data sources, leading to increased level of effort. Lastly, for AMU surveillance variable between the two coun- despite the high burden of disease attended to in hospi- tries. The costs could be higher or lower when applied to tal outpatient departments (OPDs), the available WHO the context of hospitals in LMICs. However, if capacity AMU surveillance tool is only applicable in the inpatient is built at the hospital level, these costs could be signifi - department. The Uganda Health Sector Performance cantly lowered. For example, the hospitals do not have Report of 2019/2020 showed a cumulative attendance to incur costs on travel, lodging and a workshop to train of 49,995,720 cases and 2,069,310 cases in the OPD and data collectors if capacity is built inhouse. In Uganda, inpatient wards respectively . The current inability hospitals are currently using the Primary Health Care to collect OPD AMU data creates gaps in data and may fund to run their AMR control activities, in addition to bias AMS interventions, leaving OPDs behind. Tools using the same funds to support other related activities for AMU surveillance in OPDs have been developed for like community outreach, water sanitation and hygiene use in other countries and should be adopted for use in and health promotion. However, these funds are inade- LMICs . quate, and gaps exist in financing AMR control activities . Limited AMS and AMU surveillance technical expertise in the health facilities Recommendations for addressing AMU Conducting AMU surveillance requires a skilled work- surveillance challenges in Tanzania and Uganda force, with multidisciplinary skills, including epidemio- Despite these challenges, some solutions are pro- logical, clinical, and pharmaceutical knowledge that have posed for consideration to build a sustainable structure expertise in the surveillance methodology. For example, for AMU surveillance in both countries (Table 1). We in our experience, the interpretation of diagnosis and apply the Potter and Brough model of systematic capac- indication required a medical doctor or nurse with famil- ity building to make recommendations for specific iarity in interpreting indications to be part of the team. actions across the board, that if implemented could build Kiggundu et al. Antimicrobial Resistance & Infection Control (2023) 12:9 Page 4 of 8 Table 1 Recommendations for systematic capacity building for AMU surveillance in Tanzania and Uganda * National level Health facility Expense Cost of PPS for Cost of PPS for recommendation recommendation antibiotic use in 6 antibiotic use in 13 Tanzania Hospitals Uganda hospitals (USD) (USD) Structure, Systems, and Strengthen AMU Hospital AMS teams roles surveillance of the AMS TWC National plan Hospital AMU plans Training data collectors Strengthen the imple- Appoint hospital com- Participants per diems, 6555 2493 mentation of policies mittees meals, transportation and regulations on antibiotic use Standard operating Routine monitoring of procedures antibiotic use to be part of antibiotic steward- ship program Advocacy Data collection activities Identify resources Partner engagement Per diems & accom- 11,474 5,342 modation Private sector engage- Transportation 11,474 5,342 ment Staff and Infrastructure National plan for AMR Set up hospital AMS Stationery 421 1,521 education, including programs both pre-service and Hospital AMS teams in-service trainings set up Implement AMS quality improvement projects Skills Enforcement of manda- Integrated training Data analysis (consult- 10,530 10,000 tory CPDs on AMR for ant) annual licensing Strengthen accredita- Create AMR awareness tion and licensing Tools Standardization of tools Electronic tools Automation of tools Avail data on AMS Aligning tools with Develop tools for data existing HMIS collection in the outpa- tient departments Systems for data sharing Total 38,838 24,945 sustainable systematic capacity for AMU surveillance. addressed. To achieve this, it is important that a system- Using this approach could also have a “spillover” effect atic approach to capacity building that addresses key on other AMR containment efforts in both countries and structures, systems, roles, staff and infrastructure, skills other LMICs. and tools  is adopted and applied to all the building blocks . The Program is using the USAID Pharma - Apply systematic capacity building targeted ceutical Systems Framework and the WHO Benchmarks towards a whole of approach health systems to implement key activities that are aimed at building sys- strengthening for AMU surveillance tematic AMU surveillance capacity in both countries [12, To build sustainable AMU surveillance, there is need to 15, 30]. apply interventions across all the WHO building blocks of a health system . Human resource needs, gov- Use a phased/gradual implementation approach ernance, service delivery, financing, health informa - Our Program’s use of a gradual implementation approach tion systems and medical products components of the has shown to be successful for similar settings in low health system that apply to AMU surveillance must be resource settings, as recommended in the WHO GLASS K iggundu et al. Antimicrobial Resistance & Infection Control (2023) 12:9 Page 5 of 8 manual for early implementation . This approach is need to support set up of an AMU surveillance work- allows for consideration of local context, national priori- ing team and institutionalize this team into government ties, available resources and has successfully been used structures. At the health facility level, there is need to by Uganda to build capacity under the GLASS . In establish and strengthen AMS teams as part of the drug Uganda, a starting point could be rejuvenating the appro- and therapeutics committee which will provide leader- priate medicines use unit at the Ministry of Health level ship for AMU surveillance. The Program has worked and following this up by starting AMU surveillance at with country partners to set-up AMS teams in 6 and 13 sentinel surveillance sites as capacity is gradually built hospitals in Tanzania and Uganda respectively and sup- (both technical and logistical) at the national level to ported the teams through training and mentorship. add more health facilities to the program and later man- date AMU surveillance in representative hospitals in the Strengthen the implementation of policies and regulations country. Advanced support could involve digitalization of on antibiotic prescription and use efforts, linkage or enforcement of legislation and linking Non-prescribed antibiotics are known to increase inap- data to AMR surveillance. The Program has made con - propriate use of antibiotics and increase global use and tribution to systematic capacity building through imple- misuse , with the highest non-prescription use menting priority WHO Benchmark actions for IHR that found in LMICs, at between 19 and 100% in some cases would lead to an advanced capacity. Examples of WHO . Coupled with poor adherence to treatment guide- Benchmark actions completed with program support lines in Uganda , this practice compounds access include assessment of policies for antibiotic stewardship to unauthorized parallel markets for antibiotics , in both countries, writing of a NAP for AMS and con- making AMU surveillance more problematic. Uganda ducting assessment of systems for AMU surveillance in has recently assessed policies and regulations on anti- Tanzania and Uganda, respectively. biotic stewardship—a key WHO Benchmark activity, with the activity ongoing in Tanzania. There is a need Strengthen leadership and governance for AMU address the identified gaps in relation to AMU surveil - surveillance at all levels lance, strengthen implementation of existing regulations Strengthening leadership and governance for AMU sur- on antibiotic utilization and access, over-the-counter veillance is critical for AMR control . non-prescription access of antibiotics in both countries At the national level, an AMU surveillance team under and control of antibiotic use in the veterinary sector. In the AMS multisectoral TWG should be appointed Tanzania, the Program supported the development of an and facilitated (technical expertise, capacity building, AMR NAP and adaptation of the WHO AWaRE catego- resource allocation) to enable them to understand and rization. This in turn was integrated into the Tanzania support the implementation of the long-term vision for Standard Treatment Guidelines and National Essential AMR control. These bodies should take a major role in Medicine List. vertical coordination, upstream with the MSC-AMR body and downstream with facilities and communities. Build stronger data systems with relevant tools The AMS TWG can catalyze funding advocacy, coordi - in cognizance of the local country context nation, research, reporting, dissemination, overall coor- First, there is need to conduct review of existing HMIS dination, link AMU surveillance to AMR surveillance for AMU surveillance and use the findings to inform the and laboratory capacity, and facilitate the use of data for development of relevant electronic tools for AMU data decision-making. As part of strengthening leadership, collection. The WHO PPS tools should also be digital - there is an urgent need for approval of national AMU ized and incorporated into the data collection tools at surveillance plans, which clearly define roles and respon - the health facilities. In Uganda, linking currently avail- sibilities and provides a platform for establishment of a able tools on AMU surveillance into existing HMIS tools governance structure. The TWGs and AMS teams could like the Pharmaceutical Information Portal, Supervision catalyze the South-to-South Learning. For example, Tan- Performance Assessment and Recognition strategy  zania conducted their AMU surveillance before Uganda and the District Health Information System- 2 (DHIS-2) and as part of capacity building for Uganda, a technical should be considered. Similarly, data collection through exchange was organized between the Program’s teams the DHIS-2 can be strengthened in Tanzania. The WHO - where the Tanzania team shared their experiences. The NET software  could be modified to include a module Program supports multisectoral TWGs in both coun- for AMU surveillance in both countries. The WHONET tries; for example facilitating data sharing through quar- can as well be integrated with the national DHIS2 system. terly meetings in both countries and publication of a Through integration, challenges of unavailability of data, newsletter in Uganda . However, as a next step, there missing data and poor data quality could be addressed Kiggundu et al. Antimicrobial Resistance & Infection Control (2023) 12:9 Page 6 of 8 while also creating a system that allows for data sharing a need for alignment of approaches, to generate data at the health facility and the national level. Additionally, on a regular basis to inform interventions (for exam- consideration could be made for adapting the Interna- ple the 2023 goal of 60% antibiotics used being from tional Classification of Disease for coding of diagnosis in the Access category ), but also share globally to both countries and other LMICs. Such a system will allow inform response efforts. The current approaches to for similar nomenclature of diagnosis, bring clarity on AMU surveillance do not allow for systematic data col- indication of antibiotics, and allow for progress towards a lection that is representative to allow for a comparison clinical coding surveillance system, which would support of trends of antibiotic use. Through systematic capac - systematic surveillance and minimize human resource ity building, health financing bottlenecks should be needs and the costs of surveillance. Lastly, robust sys- addressed including defining the government, private tems should be developed to collect data on AMU from sector engagement, reducing donor dependency of the OPDs. In Uganda, the Program has applied the WHO the AMR program, while maintaining relevant inter- methodology on drug indicator survey to collect data national collaborations and partnerships. Lastly, data from the OPD . should be used for action to gradually build capacity for AMU surveillance and AMR containment. Although the surveillance of AMU should be guided Support knowledge and skills transfer at all levels by the national AMU surveillance plan, both countries of the health care system are not implementing these plans. This will be critical It is urgent to build a critical mass of experts to support to foundation building for the national program, sup- AMU surveillance at both the national and health facil- port long-term sustainable capacity building, enable ity level through training and mentorship programs in resource mobilization and allocation, define key roles both countries. To overcome the observed lack of techni- and responsibilities, and define governance mechanism cal capacity for AMU surveillance among health workers, for data collection, management, and sharing while a competency-based curriculum on AMS incorporating supporting activity implementation at the sub-national AMU surveillance, with additional educational inter- levels and health facility level. Along with this, there ventions like continuous medical education, mentor- is a need for agreement on the best methodological ships, and continuous professional development sessions approach for data collection, adopting or developing should be developed for in-service health profession- simple tools that are applicable in resource-constrained als. This would be in line with the WHO framework settings like Uganda and Tanzania. The standardization on health worker training for AMR . Additionally, of existing methodologies in the context of LMICs is important components on AMS and AMU surveillance also critical to enabling the generation of relevant data. should be introduced in pre-service curriculum and their Most of the currently available tools, although devel- implementation supported during houseman years or oped for use in LMICs may not be applicable to both internship training to provide a foundation for long term countries, due to unique human resource and health learning for AMR. The facility technical experts will sup - system challenges. port the development of contextualized AMU metrics, In countries where infectious diseases, including bac- monitor activity performance, validate methodologies, terial infections, remain a major cause of morbidity and and guide operational research. Lastly, there is need to mortality, vis a viz an increasing burden of AMR, it is develop a culture of AMS at the health facilities. This can imperative that we implement to understand the drivers be achieved through implementation of quality improve- of AMR. Proper AMU surveillance systems will inform ment plans, training, and mentorship. In Tanzania, the efforts toward proper access to antibiotics to treat infec - Program is implementing quality improvement plans in 6 tious diseases and provide critical information to sup- hospitals. In Uganda, the Program has cumulatively sup- port optimal use to combat the emergence and spread of ported 131 facility-based continuous medical education AMR. The recommendations made in this article should sessions benefiting 2,152 health workers, 2 continuous support the development of a strong sustainable national professional development sessions and 34 onsite mentor- AMU surveillance program for both Tanzania and ship visits. Uganda and other LMICs. Supporting the implementa- tion of these recommendations will enable the country to Conclusion progress on the WHO Benchmark 3.4, capacity 3, and 4 With increasing global efforts to combat AMR, there outlined above . is a need for comparative data from countries on AMU surveillance. Various methods and approaches to AMU Acknowledgements The authors would like to thank the following individuals for their input into surveillance have been applied in both countries. AMU this work: Doris Lutkam, Samir Saitoti, Siana Mapunjo, Emiliana Francis, Talhiya surveillance programs are in their infancy and there is K iggundu et al. Antimicrobial Resistance & Infection Control (2023) 12:9 Page 7 of 8 Yahya all from Tanzania and Dr. Josephine M. Oyella (St. Mary’s Hospital, Lacor), 5. WHO. Global action plan on antimicrobial resistance. 2015. http:// www. 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Antimicrobial Resistance and Infection Control – Springer Journals
Published: Feb 9, 2023
Keywords: Antimicrobial resistance; Antimicrobial use surveillance; Capacity building; Health system; Africa; Global health security; Point prevalence survey; Tanzania; Uganda
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