Administrative and infrastructural support for AMS programs
Twelve hospitals (70.6%) had senior management teams that had not formally identified AMS as a priority objective for their institutions and included it in their key performance indicators. Table S1. Fifteen hospitals (88.2%) reported that there was no dedicated, sustainable, and sufficient budget to support AMS activities, and no documentation that defined the roles, areas of collaboration, or responsibilities of the AMS team. Fourteen hospitals (82.4%) did not have sufficient staff to conduct AMS activities, thirteen hospitals (76.5%) did not have a document that defined the areas where the AMS team would collaborate with the infection prevention and control (IPC) team. Table S2. Eleven hospitals (64.7%) had AMS committees that did not regularly document the minutes of their meetings, ten hospitals (58.8%) had multidisciplinary AMS teams to implement strategies, a dedicated leader to spearhead the activities, and involved clinicians, nurses, or pharmacists (other than those in the AMS committee) in AMS activities. Table S2. The Medicines and Therapeutics Committee was present in eight hospitals (47.1%), the infection prevention and control (IPC) and patient safety committees were present in three hospitals (17.6%), two hospitals (11.8%) had other pharmacy committees to handle AMS activities (the Pharmacy and Therapeutics), while one hospital (5.9%) had a pharmacovigilance committee that focused exclusively on appropriate antimicrobial use.
From the qualitative perspective, one key informant pointed out that AMS was done to ensure appropriate use of antimicrobial agents.
“AMS is basically the strategies that have been put in place to improve appropriate use of antimicrobials. To make sure that they are used well, to minimize side effects and eventually the total cost of antimicrobial treatment because recently there’s been an increase/surge in AMR. Therefore, Antimicrobial stewardship programs are helping to mitigate this challenge such that we can preserve the antibiotics that we can use. Stewardship is basically strategies that are put in place to minimize AMR, which eventually lowers the costs of antimicrobial therapy”.
However, the other key informant was not conversant with AMS:
AMS?, I must be very honest, I am hearing this term for the first time. But the way I would imagine, it has to do with taking responsibility to make sure that first we have the right antimicrobial medications to use, and we have measures in place to ensure that they are not misused to lead to undue resistance. It’s the biggest threat, antimicrobial resistance. So, stewardship, I think the institutions and the different actors must take responsibility to ensure that we minimize as much as possible on microbial resistance and make sure that we have the right antibiotics and medications to deal decisively and effectively with the microorganisms we encounter in our existence. We all have a role to play when it comes to AMS.
When asked whether there were any government guidelines/policies that supported AMS activities in private hospitals, one key informant (KI I) had this to say:
Yes. In private hospitals, we have guidelines like the Uganda Clinical Guidelines (UCG), 2016 edition. These are the guidelines that we must use and are available for prescribers to follow and use to ensure that the medicines generally are properly administered to patients. In this one, we try to make these booklets available to all the prescribers across public and private health facilities. We have soft copies available online. Every 3–5 years the UCGs are revised. All stakeholders are involved in this revision including private service providers. All these policies are geared towards preventing resistance and preserving antibiotics in use. National Drug Authority (NDA) works closely with the Ministry of Health Uganda. It’s under the ministry. It’s the arm of the ministry that is regulatory to protect the public through regulation of medicines. So, the strategy for AMS is one that we get from the plan that the Ministry of Health has developed, of which the NDA has fully contributed to. NDA works hand in hand with MoH on any programs in both private and public hospitals. Also, there is the AMR-NAP 2018–2023 that elaborates the strategies in place to promote antimicrobial stewardship. The policy used by MoH covers all stakeholders both in public and private health facilities. There is also the National Infection Prevention and Control Guidelines with the latest version of 2013 that also feeds into the ASPs. The Uganda Clinical Guidelines (UCGs) 2018 to provide guidance on the use of antimicrobials in treatment of diseases. NDA ensures optimal access and use of antimicrobials in the public and private sectors with guidelines on importation and exportation of antimicrobials. Registration guidelines for antimicrobials before they can be registered in the country. Licensing guidelines for facilities that sell antimicrobials. Licenses are now being given to pharmacies in private hospitals as well. Supervision performance assessment and recognition strategy (SPARS) is being implemented at district level to examine human health facilities application of these guidelines. Establishment of a multi-sectorial committee to oversee and provide overall coordination of the implementation of this AMR-NAP which is known as the Uganda National Antimicrobial Resistance Committee (UNAMRC)
Composition of the teams, frequency of meetings, availability of expertise, training opportunities, and training delivery methods in the study area
Most AMS members were clinicians (64.7%), pharmacists, (58.8%), and medical laboratory scientists (52.9%). Others included nurses (47.1%), infection prevention and control personnel (41.2%), and surgeons (35.3%). Data analysts were the least represented in the AMS team. Only six (35.3%) of the studied hospitals held quarterly AMS meetings, four (23.5%) held monthly meetings and only one (5.9%) held meetings weekly. All the hospitals not only had access to laboratory/imaging services, but also availed the results in a timely manner to support the diagnosis of common infections. Table S3. Sixteen hospitals (94.1%) had access to healthcare professionals (medical doctors, pharmacists, nurses etc.) who were specialized in infection management (diagnosis, prevention, treatment, and stewardship) and were willing to constitute an AMS team. Table S3. However, staff in one hospital were not ready or willing to constitute an AMS team. Induction training was conducted on clinical staff in twelve hospitals (70.6%), with nine of these including training on AMR and IPC. Six hospitals (35.3%) conducted AMS training up to four times in a year while two hospitals (11.8%) had training twice a year. However, two hospitals (11.8%) had no records of the general number of trainings conducted yearly. Figure 1.
Thirteen hospitals (76.5%) conducted AMS training online while four (23.5%) held physical or face to face meetings. Seven hospitals (41.2%) conducted in-hospital training through continuous medical education (CME) delivered by staff within the facilities and six hospitals (35.3%) received training from pharmaceutical companies. Training in three hospitals (17.7%) were supported by the Ministry of Health, Uganda, and training in two hospitals were supported by the National Drug Authority (NDA) and the Pharmaceutical Society of Uganda (PSU). Doctors, surgeons, and pharmacists in seven hospitals (41.2%), nurses in eight hospitals (47.1%), and other clinical staff in nine hospitals (52.9%) had not received any AMS training in the last one year. Figure 2. Only four hospitals (23.5%) had more than ten doctors and surgeons who had been trained on AMS within the last year, seven hospitals (47.1%) did not train any of their nurses on AMS but at least one pharmacist in nine hospitals (52.9%) received training on AMS in the last one year. Figure 2.
More than ten doctors and surgeons in six hospitals (35.3%) received IPC training and more than ten nurses in seven hospitals (41.2%) received IPC training in the last one year. Figure 3. Moreover, up to ten pharmacists were trained on IPC in ten hospitals (58.9%). Six hospitals (35.3%) had not trained any of the other clinical staff on IPC in the last one year.
Regular reporting, feedback, and monitoring and surveillance of AMS activities in the study area
Eight hospitals (47.1%) monitored the quantity of antimicrobials prescribed/ dispensed/purchased at the unit and/or hospital level. Thirteen hospitals (76.5%) reported that their hospital stewardship programme did not monitor compliance with one or more of the specific interventions put in place by the stewardship team, three hospitals (17.7%) monitored antibiotic susceptibility patterns of key bacteria but none of the hospitals had conducted a point prevalence survey (PPS) for antimicrobial use within the last year. Table S4. Thirteen hospitals (76.5%) reported that they did not have hospital-specific reports on the quantity of antimicrobials prescribed/dispensed/purchased and did not share any feedback to prescribers, twelve hospitals (70.6%) did not share facility specific reports on antibiotic susceptibility rates with prescribers, and ten hospitals (58.8%) did not communicate the results of audits/reviews of the quality/appropriateness of antimicrobials with prescribers. Table S5.
When KI 2 was asked whether the hospitals reported any hospital AMS related data to the ministry of health the informant had this to say:
There is no policy requirement for them to report. As I mentioned before, they give us reports on general medicines and supplies, use, storage, availability, and proper use. That is all they share with us.
When asked whether there was monitoring and evaluation standards for AMS at NDA level, the key informant (KI 1) remarked:
That information comes in form of complaints and there is a whole pharmacovigilance arm that receives ADR complains in relation to a particular drug. So that is the kind of information that we receive from hospitals, complaints about antimicrobials which are not working in patient treatment. So, it is against that information then that NDA goes on to do further research, maybe do quality tests, maybe do a real study to verify this information. Recently, we have just completed a study on ceftriaxone use, where the public was complaining that the ceftriaxone in the market is not working.
In addition, quality tests were done, and the drug passed the quality tests. So, as NDA we did a study to find out if there was anything more that could be causing the treatment failure. And indeed, from our findings we realized that there is also an aspect of irrational use, where it’s the way the drug is used not per say the quality or the brand vs generic. The drug is working but now we should be able to emphasize rational use in hospitals, remind health workers on how to use antimicrobials, give the right doses and encourage patients not to miss doses and to complete their treatment regimens. So, that is the way we get information and that is how we respond in terms of stewardship. But of course, the other arm, because we are stakeholders in importation, we have data on what has come into the country and against that we can be able to gauge probably consumption and through that maybe by modelling and other mechanisms, we can be able to find out resistance patterns or over usage or irrational use, etc.
When asked whether there was monitoring and evaluation standards for AMS at MoH level, the key informant (KI 2) remarked:
“The structures are there across different facilities. We call them ‘quality improvement teams’ and their roles are also included, and we are supposed to handle most of these issues to do with medicines and supplies, including AMR. But of course, one of the key issues is building capacity for them, to appreciate how they need to do this and to be responsive and give us the appropriate data we need to guide for decision making, that is, informed decision making. So, what is being done can be seen mostly in public facilities but should be extended to private health facilities. They should also be given clear terms of reference and appropriate tools for them to monitor AMR and to report on a regular basis. So, what is done; structures are there, some are functional, some are not very functional, and we think it’s an opportunity we can use now to address this issue of AMR.”
Actions to improve responsible antimicrobial use
Twelve hospitals (70.6%) had up-to-date recommendations for infection management (diagnosis, prevention, and treatment), eight hospitals (47.1%) had established AMS protocols (restricted antimicrobial list, IV to oral policy) that were ratified by the hospital administration, fifteen hospitals (88.2%) had infection prevention and control protocols (hand hygiene, WASH) that have been ratified by the hospital administration, eleven hospitals (64.7%) did not have regular IPC focused ward rounds, and twelve hospitals (70.6%) had local/hospital specific antimicrobial prescribing guidelines. Table S6. Five hospitals (35.3%) had three tools on AMS, six hospitals (35.3%) had two guidelines for IPC/AMS, one hospital (5.9%) had only one tool, and five hospitals (35.3%) had no IPC/AMS tools. Respondents in fourteen hospitals (82.4%) were aware of national or regional guidelines on the management of infections, respondents in ten hospitals (58.8%) were not aware of any national campaign on AMR awareness and had not come across any national newspaper articles on antibiotic awareness, respondents from nine hospitals (52.9%) were not aware of the World Antibiotics Awareness week and respondents in sixteen hospitals (94.1%) had not come across any other initiatives on antibiotic awareness and resistance other than those listed in the checklist. However, a respondent in one hospital (5.9%) had gotten information on antibiotic awareness and resistance from other sources, which were identified as medical representatives. Table S7. Respondents in fourteen hospitals (82.4%) were aware of national or regional guidelines on the management of infections, respondents in eleven hospitals (64.7%) had received awareness from professional organizations, conferences/events aimed at tackling AMR, and water and sanitation and health (WASH) initiatives with global hand hygiene/WHO. Respondents in four hospitals (23.5%) reported receiving awareness from TV or radio. Table S7.
Ten hospitals (58.8%) had put in key actions in the past one year to combat AMR and/or promote judicial use of antibiotics, while six hospitals (35.3%) had not undertaken any key actions in the past year to combat AMR and promote the judicial use of antibiotics. A respondent in one hospital (5.9%) was unsure if their hospital had undertaken any actions to combat AMR and promote the judicial use of antibiotics. Table S7. The key actions reported included conducting training on AMS, preparing pre-authorization drug lists, conducting peer review workshops on prescription and prescribing habits, and providing mandatory feedback to prescribers on good prescribing habits. Others included putting restrictions on the prescription of some drugs, ensuring that prescriptions emanated only from authorized clinicians, ensuring there were pre-treatment laboratory investigations, and strengthening laboratory capacity on culture and sensitivity. Other key actions included strengthening the use of prescribing guidelines on antibiotics and monitoring antimicrobial consumption from the pharmacy department. One hospital mentioned that the key action they had undertaken was the commissioning of a hospital Drugs and Therapeutics Committee within the last year, to promote judicial use of medicines within the hospital and combating AMR.
Barriers to Antimicrobial Stewardship in Private Hospitals
Qualified personnel did not have enough time to perform stewardship activities (76.5%), poor resource allocation (58.8%), giving in to patient demands or beliefs by healthcare workers (52.9%), and the high cost of antibiotics (47.1%) were the major barriers to AMS in the study area. Table 1.
Table 1
Barriers to the implementation of antimicrobial stewardship programs in private hospitals in Kampala, Uganda
| Main barriers to AMS in Private Hospitals | n (%) |
| Lack of qualified personnel | 1 (5.9) |
| Qualified personnel do not have enough time to perform stewardship | 13 (76.5) |
| Lack of motivated or engaged staff | 5 (29.4) |
| Lack of funding | 10 (58.8) |
| Lack of support from hospital management | 3 (17.6) |
| Insufficient microbiology laboratory capacity | 5 (29.4) |
| Inadequate use of the microbiology laboratory | 2 (11.8) |
| Poor quality of antibiotics | 7 (41.2) |
| Regular shortages or stock-outs of essential (“Access”) antibiotics | 3 (17.6) |
| High cost of antibiotics | 8 (47.1) |
| Lack or unavailability of practical, evidence-based, local guidelines | 7 (41.2) |
| Lack of trust in local guidelines | 3 (17.6) |
| Lack of cooperation from prescribers | 7 (41.2) |
| Lack of knowledge on good prescribing practices among clinicians | 4 (23.5) |
| Lack of expertise and training in AMS within the AMS team | 6 (35.3) |
| Lack of confidence in hospital infection prevention and control (IPC) processes | 0 (0.0) |
| Lack of information technology support | 4 (23.5) |
| Patient demands or belief | 9 (52.9) |
| Other | 2 (11.8) |
| From a qualitative perspective, some of the challenges reported by the hospitals were reflected by one of the key informants who said: |
“One clear challenge that has come out already is non-functional MTCs, which makes it hard to monitor AMS activities in hospitals. We are finding ways to motivate these MTCs to be able to report in terms of maybe infrastructure and logistics.
Costs involved in health facilities for culture and sensitivity testing are high. The high costs can lead to hospitals by passing these tests, or sometimes the patient may not afford it. Shortages in supplies maybe a challenge.
The pressure that comes with business versus the right thing to be done especially in private hospitals. Because here, someone is looking at sales at the same time they must handle the aspect of treatment. So, we have issues like for instance, giving a particular antimicrobial not because it is required but because it is a drug that is going to bring money into the business. That is a challenge, and I call that pressure to make sales.
In line with that another challenge is patient satisfaction. You can find a scenario where patients prefer certain products and will push the prescriber to give that drug, not so much that they need it but because they think it works for them. And the prescriber will bend to the will of the patient and disregard appropriate antimicrobial use.
Therefore, strategies that should be able to bring a balance between businesses OR between what the patient needs vs what should be done is still a challenge especially in the private sector. In the public sector that challenge can be easily managed by prescribing and dispensing according to supplies and guidelines