Several themes were identified while exploring data on the perspectives of health workers on the influencers of occurrence, transmission, and management of AMR caused by several implicated bacteria. Themes, sub-themes, and quotes from the study were reported in this research article. The main themes reported included; occurrence and its determinants; spillover and transmission dynamics as well as management of AMR. The study findings are presented according to their respective themes and related quotes from the participants (Table 2).
Table 2
Organizing and basic themes that emerged out of the analyzed data
Organizing themes | Basic themes |
Occurrence of AMR | Local and professional understanding of AMR |
The burden of and vulnerability to AMR |
One health nature of AMR |
Factors influencing the occurrence of AMR | Antibiotics are being given for the wrong disease |
Herbal medicine contributes greatly to AMR |
Human drugs used in animal treatment and vice versa |
Treatment before diagnosis |
Self-medication |
Failure to observe drug withdrawal periods |
Poverty forces individuals to bargain on the number of drugs to take home (dosage) |
Spillover and transmission dynamics of AMR | Environment, fertilizers, and foods of animal origin are great Sources & reservoirs of AMR |
Cultural norms, values, and practices |
The closeness between humans and animals |
Zoonotic and reverse zoonotic nature of AMR pathogens |
Management of antimicrobial use and antimicrobial resistance |
Contribution of key actors in AMR occurrence and management | Policies, legal and regulatory framework laxity |
Neglect of service extension workers and community support organizations |
Healthcare facilities, pharmacies, and laboratories play a critical role in the AMR cycle |
Climate change and technological advancement |
Strategies to prevent the occurrence and transmission of AMR | Sensitization to bridge the knowledge gap |
Proper diagnosis before treatment |
Enforcement of AMR prevention and control strategies |
Regulation of antimicrobial use in humans and animals |
One health approach to eliminating silos |
Occurrence Of Antimicrobial Resistance
In this study, occurrence referred to situations in which communities believed and experienced the existence of AMR. The profession of an individual determined how they understood and promptly explained the meaning of AMR, i.e., some health workers were more knowledgeable than others. Professionals from the animal sector provided a better description of AMR occurrence and development compared to their counterparts. The natural phenomenon and selection pressure or gene exchange were reported as the three main forms of AMR occurrence. Indeed, veterinarians related AMR development to both the underuse and overuse of antimicrobial agents since such practices normally create selection pressure for the organism which ultimately contributes to the development of resistance mechanisms thus rendering drugs ineffective for use.
Even though health workers at district and sub-county levels revealed a high level of awareness, the community-based health workers, VHTs, during the FGDs could not explicitly explain the concept of AMR. Despite this, the VHTs could ably testify on the problem of drug failure and expressed a high level of willingness to learn about these “superbugs”.
Our people in the communities are having these issues of drugs not working on them and their animals, they trust us, but we can’t explain why this is happening. So, our thinking is if we could be sensitized about how this happens and how we can avoid it before things get worse… (FGD04, P2, S4).
Worth noting is the consensus between all KIIs and about half of the FGDs on reporting a high perceived threat from AMR resulting in hard-to-treat infections among both human and animal populations. Most KIIs believed that persons who are immunocompromised and those in professions that expose them to these biological hazards were more at risk. Such categories of high-risk groups reported include, veterinary doctors, laboratory technologists, butchers, and restaurant workers among others. One of the key informants indicated that:
…affected most are those in high-risk areas like healthcare settings, handlers of animals, immunocompromised, people who prepare food of animal origin, and those who work with environmental waste are a risk group because they deal with the environment where these resistant organisms usually occur (KII02, S4).
Human health professionals believed that despite their limited knowledge of animals, there must be a similar resistance challenge in the livestock sector as it is in the human sector. Most KIIs report that the AMR is a broader concept and encompasses animals, humans, and perhaps the environment.
This AMR thing is too broad and can even affect healthy animals and humans even though I am not well versed with what happens in the animal world. I think as it is in humans, it can also be in animals and farmers must buy more drugs in case treatment does not work (KII03, S1).
Factors influencing the occurrence of AMR
The availability of substandard and counterfeit antimicrobials was suggested as a significant contributor to the occurrence of AMR. Several other factors were reported to be influencing the occurrence of AMR among human and animal populations. These included; self-medication, negligence of the medical practitioners and veterinarians, use of human drugs for animals and vice versa, as well as humans, staying with their animals in habitable rooms. Wrong medication for a disease, incomplete doses; treatment before diagnosis were also reported.
Over-the-counter sale of antimicrobials has greatly led to self-medication which has ultimately culminated in AMR. As a result, the medical personnel are left with no option but to resort to “reserve drugs” to manage infections and diseases. FGD participants, however, blamed the professionals, especially human doctors. They revealed that medical doctors do not take their samples to test for what they are suffering from, but rather just give medicine and they believed that this at many times makes the illness resurface which may imply that the drugs did fail to work.
… a very big problem because these days anti-microbial drugs are routinely used and easily acquired, where someone has simple flu and buys amoxicillin. We see this often where first-line drugs e.g., ampicillin, amoxicillin no longer makes a change to any sick person hence switching to third-generation drugs (KII 01, S1).
But sometimes we got to the health centers, and the doctor does not even touch you to feel your sickness, they don’t take any sample to check so you also leave the hospital disappointed even when you get drugs, they at many times do not work… (FGD03, P07, S3).
It is important to note that key informants in both the human and animal health sectors agree that some human and animal drugs are interchangeably used at a community level. For example, human drug dispensers (pharmacists) report that farmers come and take drugs such as amoxicillin, Artemether / Lumefantrine (coartem), and chloramphenicol to treat their calves and chicks. Nevertheless, cases of humans using animal drugs to treat rare infections such as sexually transmitted infections (STIs) were also revealed. FGD participants however report that veterinarians send them to go and buy drugs from human drug outlets to treat their sick animals claiming that they are fine with using them since they are effective.
…even the veterinary doctors to use those human drugs to treat our animals. For example, ARVs are not only used in chicken but in pigs too and to a greater extent (FGD 01, P3, S1).
Just remembered, we have clients who buy amoxicillin, coartem, and chloramphenicol to treat chicken and when we advise it’s not for animals, they insist and take for their calves and chicks (KII07, S02).
The common one we use is penicillin, used in animals to treat cases of injury, and cough, and used in humans, it is used mostly to cure gonorrhea and syphilis. So, people go to animal drug shops to get the drug to cure that illness. Then tetracycline is also used in both humans and animals (KII 09).
KII participants reported that many of the community habitats are below the poverty line and therefore cannot afford private healthcare facility bills even though these would be their first choice of preference. They indicate that the government facilities sometimes lack essential drugs and diagnostic tools and at many times they require a patient to get extra support from a private facility. To overcome such situations, most community members have resorted to using traditional medicine (herbs) as an alternative to antibiotics since they believe herbs have no prescription limits and are easily accessible within the environment.
Some of our patients use herbal medicines, some are healed, others heal but the infections re-occur so by the time they come, they are not responding to certain drugs. Therefore, we are not sure whether their local medicines have active chemicals that perhaps lead to AMR. (KII10, S3).
For the animals that are treated with antibiotics, farmers do not know the right doses to use and fail to recognize the drug withdrawal period precautions. Failure to observe drug withdrawal periods leads to effects of antimicrobial residues in animal-based foods such as milk, meat, eggs, therefore, leading to AMR.
A farmer can give penicillin to a cow or oxytetracycline. Yes, the drugs are right, but we don’t know if the given doses are right or not, plus they don’t observe the withdrawal periods. In the end, they give people milk with drug residues, so these small doses make the pathogens stronger hence being able to resist the drug (KII09, S2).
Spillover And Transmission Dynamics Of Amr
Spillover refers to the spread of AMR from humans to animals, animals to humans, humans to the environment, or animals to the environment and vice versa. The transmission would imply the spread within the same category i.e., from one environment to another, humans to humans, and animals to animals. Several factors were reported to be crucial in these dynamics and these included; contaminated food value chain, zoonotic and reverse zoonotic nature of the pathogens, the role of environmental reservoirs, organic fertilizers, and close interaction at the human-animal-environment interface among others.
After thorough sensitization of the VHTs during the FGDs, some participants thought that foods of animal origin could be the silent “keepers” of these drug-resistant germs. They believed that the food value chain especially that of animal origin is a probable risk for antimicrobial-resistant bacteria and is associated with serious health-related consequences. However, they recommended that thorough cooking of these animal-based products can save you from these resistant germs since they fear heat.
I think humans who feed on treated animals or their products like milk and eggs are affected health-wise and economically…but I think if we cook our meat so well and boil milk for chronic diseases such as Brucellosis will not get us (FGD 02, P5, S1).
The majority of the animal health workers highlighted that these diseases end up affecting humans as well hence zoonotic. The diseases have the potential to spill over from the human population back to the animals hence reverse-zoonotic in nature. Such diseases have also continuously not responded to antibiotics being given. Findings of this nature never came up even with continuous probing with the FGDs.
When I had just started practicing, tetracycline was working, unlike these days. The most worrying thing now is, we were recently told that some of these animal diseases can affect humans… (KII01, S1).
Overexposure of animals and humans to antibiotics may result in AMR which may, in the end, be disseminated into the environment and the cycle may continue. Most KIIs from S4 and S2 sub counties recognized the role the environment plays in the global spread of clinically relevant AMR in different forms such as water sources, dumping sites for clinical waste, and playing grounds for children among others. One key informant asserted that:
Most animals get AMR from fertilizers. Also, if sick animals drink water and or defecate in the same water, it gets contaminated then the quality of that water is compromised. Humans can also get infections through that water, so that is how the environment can lead to the spread of those diseases (KII04, S4).
FGDs in S2 and S4 reported that some community members stay with livestock in their households. In addition, cultural norms, beliefs, and values underlying animal production also heavily contribute to AMR spillover and amplification. They believed that this would lead to spillover of any infectious pathogens including the resistant types from animals to humans and vice versa.
Keeping animals inside the house leads to the transmission of diseases, it brings about disease spillage. “People should learn how to care for their animals without getting diseases from them… (FGD04, P2, S4).
… are cultures where people believe that if you blow air into the vulva of a cow, it will release more milk. In the process, you end up contracting bacteria… (KII05, S1).
Management Of Antimicrobial Use And Antimicrobial Resistance
Most human health professionals highlighted the high cases of AMR reported from communities due to the number of drug-resistant infections that report to their facilities. They believed that resistant infections could be dealt with by changing the treatment course to higher-class antibiotics, even though the prior diagnosis was overlooked. Safe husbandry practices on the side of animal health workers were thought to ultimately lead to safe homes, safe lives (animal and humans), and a safe environment. Under the management of antimicrobial use and AMR, we report the key actors, their contribution to the occurrence and management of AMR, as well as key strategies existing and those that would be ideal in the prevention and control of AMR.
Contribution of key actors in AMR occurrence and management
The laxity of policy implementation and unskilled human resources in the human, animal, environment, and food sectors have driven the escalation of AMR. The neglect of community support organizations (CSOs) to comprehend government works and working in silos by the concerned ministries, departments, and agencies (MDAs) on human, animal, and environmental issues was yet another driver for the AMR burden reported. This has increased the burden of AMR without clear indicators or early warning systems for the problems. This, therefore, calls for a dire need for multidisciplinary teams to solve the AMR challenge, especially in farming communities.
We have always required several organizations that teach us about diseases. However, if the government can work with these organizations or for example human doctors work with animals doctors to help us understand such problems like the one we are discussing…, our people would benefit and in the end help the government fight against such diseases (FGD03, P6, S3).
The majority of the KIIs noted that the health facilities including pharmacies and hospitals contribute a lot to AMR in different ways such as health workers not minding about drug handling and storage, health workers who sell drugs over the counter, and those that are not qualified. The role of health facilities has also seen patients acquire nosocomial infections from health facilities which has increased AMR among certain organisms that were earlier non-resistant. In addition, the animal production sector and climate change have also greatly influenced the increase and decrease of AMR in various ways.
Climate change has a role specifically in the issues of change in the conditions whereby places which used to be colder are now warmer and those which were warmer are now colder and this facilitates the transmission and evolution of infectious pathogens to drug-resistant nature (KII02, S3).
Technology was also reported as a key player in the AMR arena. Community health workers believed that the advancement and increased access to technology such as the internet within the country have made people shun away from visiting the health care facilities or calling veterinarians to treat their animals. They instead use search engines especially google to find a solution that they execute, and this may contribute to resistance due to poor drug usage.
…some people here no longer visit health facilities when sick, they just go to the internet, and type how they are feeling or the disease they are having then the internet will provide quick solutions to them (FGD 02, P7, S2).
Despite this downside, technology has also been recognized in the increased diagnosis of infections and their drug susceptibility profiles. This gives chance for treatment after diagnosis and thus retards the development of AMR leading to quick and positive treatment outcomes both in humans and animals. One KI asserted that:
… laboratories have been set up with up-to-date equipment that can support diagnosis of any infection in a short period. So, advancement in lab diagnosis has helped us, then the advancement in the manufacturing of drugs has also helped us … (KII03, S4).
Strategies to prevent the occurrence and transmission of AMR
Weak enforcement systems have continuously failed to regulate the sale of antimicrobials over the counter. Accessibility to drugs has been classified according to the World Health Organization (WHO) framework indicating three forms of access i.e., restricted access, common access, and reserved access. Reserved access and restricted access can’t be gotten over the counter but those with common access can be purchased in Uganda. Even though this policy is in place, the enforcement is weak since the country currently lacks well-established therapeutic committees (TCs) in hospitals thus furthering increased abuse of antimicrobials. Since this problem is recognized among human, and animal sectors, the country can begin by setting up TCs and ensuring regulation of drug use. Animal health workers should also work closely with farmers to ensure restricted use of antimicrobials if the problem of AMR must be solved.
…We have weak enforcement systems that have allowed the sale of all antibiotics over the counter, especially those with WHO-restricted and reserved access. The problem of AMR needs to be dealt with holistically from human, animal, and environmental health sectors while seeking support from the international agencies, and organizations like WHO, OIE etc… (KII12, S4).
Current practices on AMR surveillance in Wakiso district have been through registers from the district and ministry levels. Such registers are distributed to all healthcare facilities and drug-resistant pathogens are recorded to establish the level of resistance for each drug, especially among Health center IVs and above.
Currently in Wakiso we have labs for animal diagnostics. Samples are picked and sent them to the College of Veterinary medicine (COVAB) in Makerere or the National Animal Disease Diagnostics and Epidemiology Center (NAADEC) where you can diagnose resistant organisms. While humans, we have the health Centre IVs, hospitals, and central public health laboratory (CPHL) which can be able to do that (KII10, S1).
Even though there is the capacity for diagnostics, the process is seemingly expensive and unsustainable leaving prevention and control measures as the only hope in low-resource settings. The one health approach was pointed out as one of the key approaches that could be adopted in the local context of Wakiso district. This is because the approach is quite interesting since different experts come together to share knowledge and experience in solving a health challenge.
…There are plans through the One Health approach to try and set up teams and committees to try and sensitize and do a bit of research on AMR to try and increase awareness (KII08, S2).
Most veterinary and human health workers advocated for a One Health strategy in combatting AMR at the community level. Indeed, raising awareness of AMR, understanding the transmission dynamics, and encouraging people to go to the nearest health facility in case they feel sick are crucial among communities in the bid to fight AMR. Through raising awareness, a lot of sensitization from external people and those in higher and influential positions who know about AMR can influence behavior within the community. At the health facility level, respondents suggested that health workers and drug dispensers explain in detail the use of the drug before dispensing medication to the patients. It was also suggested that continuous training of health workers and follow-up of patients by health workers can influence the behavior of communities hence reduction of AMR.
The government has to make sure they implement AMR strategies; the health workers should give right drugs and give time to patients and patients to take full doses and going for diagnosis and prescription from experts (KII09).