Introduction

In 2019, 1.27 million deaths were estimated to be directly attributable to drug-resistant bacterial infections globally, with sub-Saharan Africa suffering the highest burden [1]. Inappropriate use of antimicrobials has been identified as a leading cause of antimicrobial resistance (AMR) in low- and middle-income countries (LMICs) [2]. According to the World Health Organization (WHO), understanding the current use of antimicrobials in human and animal health is the first step in developing strategies to address barriers to the appropriate use of medicines [3]. The barriers to appropriate use of antimicrobials globally are many, ranging from lack of knowledge about proper use in communities, farms, and health care facilities, to the lack of government policies and political will [4]. In addition, self-medication and premature discontinuation of antimicrobials are evident in both human and animal health particularly in low-income settings. Poor health-seeking habits where patients expect an antimicrobial either for themselves or their animals even when not required have a negative influence on practitioners’ prescribing practices in many countries including Uganda [5, 6]. In the animal sector, antimicrobials are often used inappropriately to maximise production yields and sales profits. Sub-therapeutic doses of antimicrobials are reportedly used in animal feed for increased efficiency and disease prevention in addition to treating infections [7]. In the environment, inappropriate disposal of antimicrobials within household waste, as well as in wastewater drainage channels and water bodies has been reported [8, 9]. Given the interrelatedness of humans, animals and the environment, global frameworks have at their core the use of a One Health approach which calls for integrated action across all sectors to address AMR [2, 3].

In Uganda, at least four in every ten people seeking medical care are prescribed an antibiotic [10]. Previous prevalence levels of antibiotic use range from 39% to 44% [11] in humans, and from 66% to 96% in animals [12, 13]. A recent cross-sectional study among humans and animals found a high frequency (69% in Namuwongo ward, Kampala district and 75% in Nagongera town council, Tororo district) of antibiotic use in households and farms [14]. Due to limited access to health care in Uganda such as only 72% of households living within 5 km of a health facility, individuals are likely to self-medicate with antibiotics [15, 16]. Veterinarians in Uganda have been reported to issue out antibiotics to avoid conflict with farmers who will endure financial impact due to the loss of their livestock [6]. The patterns of antibiotic use in both humans and livestock in Uganda are largely dependent on geographical proximity to health services and economic status of humans [14]. Communities that are distant from health facilities and have a lower income status generally have reduced access to antibiotics and rely on government structures [17]. These challenges all contribute to the increased development of AMR across the country. It is important to understand the rationale behind barriers to appropriate antimicrobial use so that sustainable solutions based on behaviour change principles can be developed. In 2021, WHO endorsed the UN Sustainable Development Cooperation Framework, recognising the importance of tackling AMR to achieve some of the Sustainable Development Goals [2, 18]. In response to this, Uganda developed a 5-year AMR National Action Plan (NAP) in 2018, which sets out a framework of actions to address AMR within the country using a One Health approach [19].

Literature on the trends of antibiotic use in human health care, livestock and aquaculture settings in Uganda is increasing [12, 20–22]. However, there is still limited evidence on antimicrobial access and use in humans and animals with a focus on community settings using the One Health approach [23, 24]. Indeed, vast literature on antimicrobial use in the country is primarily on humans and health facility based particularly hospitals [16, 23]. This study, therefore, assessed knowledge and perceptions on AMR, as well as practices on the use of antimicrobials in humans and animals in Wakiso district, Uganda. The results of the study could be used to raise awareness, as well as empower communities to make informed decisions and change their health-seeking behaviours to promote antimicrobial stewardship (AMS). Such data is key to inform actions for medical, veterinary, environmental, and other professionals as well as policy makers on tackling AMR and strengthening AMS through the One Health approach as stipulated in Uganda’s AMR NAP [19]. Furthermore, the findings from this study contribute to Agenda 2063: the Africa We Want which also considers One Health as a sustainable solution to making Africa safer and healthier for humans, animals, plants and their shared environment [25].

Methods

Results

Socio-demographic characteristics of participants

A total of 418 participants from eight villages participated in the study including 75.6% (316/418) females and 35.4% (148/418) aged between 18–29 years, with a mean age of 40 years (SD 16.4). Among the participants, 62.2% (260/418) were married / co-habiting, and 49.3% (206/418) had attained primary education. The majority of participants were self-employed 66.3% (277/418), and 59.1% (247/418) had an average monthly income of less than 15 US dollars (Table 1).

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Table 1. Socio-demographic characteristics of participants.

https://doi.org/10.1371/journal.pgph.0002701.t001

Knowledge and perceptions on antimicrobial resistance

Among the participants, 63.6% (266/418) had heard about AMR, mainly from family and friends 57.5% (153/266) and health professionals 30.1% (80/266). The majority of participants 70.8% (296/418) were aware that resistant microorganisms cause infections that are difficult to treat. However, 37.1% (155/418) of the participants mentioned that AMR was only a problem for people who took antimicrobials regularly. Almost all the participants 96.7% (404/418) agreed that people should use antimicrobials only when prescribed by a health professional. Furthermore, 91.1% (383/418) of the participants agreed that health practitioners should only prescribe antimicrobials when needed (Table 2).

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Table 2. Knowledge and perceptions on antimicrobial resistance.

https://doi.org/10.1371/journal.pgph.0002701.t002

Most of the participants 62.7% (262/418) thought that they should finish the full antimicrobial dose once on treatment. With reference to the last occasion when antimicrobials had been taken, the majority of participants 90.9% (307/338) reported having received a prescription, and 95.6% (323/338) had been advised on how to take the antimicrobials by a health professional. Among the 338 participants who acquired antimicrobials on the last occasion of their sickness, 13% (44/338) did not complete the full course of treatment. The main reason given for this practice was that they felt better and no longer had any symptoms 72.7% (32/44).

Factors associated with the completion of a given antimicrobial course

Using modified Poisson regression analysis, participants who were single (APR = 1.12, C.I = 1.03–1.12, p-value = 0.01) and earning more than 90 USD on average per month (APR = 1.12, C.I = 1.02–1.23, p-value = 0.02) were more likely to have completed a given antimicrobial course compared to those who were married / co-habiting and earning less than 15 USD on average per month respectively. Participants who had antibiotics at home (APR = 0.86, C.I = 0.75–0.10, p-value = 0.05) were less likely to have completed the given antimicrobial course compared to those who did not have antibiotics at home (Table 3).

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Table 3. Factors associated with the completion of a given antimicrobial course.

https://doi.org/10.1371/journal.pgph.0002701.t003

Perceptions on access to antimicrobials for use in humans

The majority of participants 87.1% (364/418) agreed that private pharmacies / drug shops nearest to their households usually had the antimicrobials they needed. Nearly half 49.0% (205/418) of the participants agreed that their nearest government health facility usually had the antimicrobials they needed. Most participants 94.7% (396/418) agreed that antimicrobials were more expensive at private pharmacies than at public healthcare facilities. The majority of participants 71.8% (300/418) agreed that their households could usually afford to buy the antimicrobials they needed. However, 45.2% (189/418) of participants reported of the need to have borrowed money or sold household items in order to pay for antimicrobials in the past. Regarding the quality of services, 81.4% (340/418) of the participants agreed that private healthcare providers in their neighbourhood were good compared to 54.9% (229/418) for government health facilities (Table 4).

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Table 4. Perceptions on access to antimicrobials for use in humans.

https://doi.org/10.1371/journal.pgph.0002701.t004

Ownership and practices relating to antimicrobial use in animals

The majority of participants 60% (251/418) reported having animals in their households. The commonly owned animals were pigs 57.0% (143/251), poultry 49.8% (125/251), goats / sheep 35.9% (90/251), cattle 32.3% (81/251), dogs / cats 4.8% (12/418), and rabbits 1.2% (3/418). Of the 251 participants who owned animals, the majority 81.3% (204/251) reported using antimicrobials among them. Most participants 70.6% (144/204) reported using antimicrobials to treat sick animals, 61.3% (125/204) to prevent animals from falling sick, while 13.7% (28/204) for growth promotion. However, 37.1% (93/251) of the participants did not know the type of antimicrobials that were being administered to treat their animals. Most participants 74.5% (152/204) stated that veterinary workers were the main source of antimicrobials and administered them to their animals. Among the 72.1% (147/204) participants who normally sought advice about their animals, the majority 91.8% (135/147) received this from veterinary workers. Of the 57.4% (117/204) participants who reported not having sold or consumed animal products within a week after medication, 46.2% (54/117) sold or consumed their animal products after a specified time as recommended by veterinary workers. In addition, most participants disposed of unwanted antimicrobials, sachets and bottles through burning 34.3% (70/204), throwing them into pit latrines, rubbish pits, or drains / open areas 38.7% (79/204), while only 18.6% (38/204) returned unused antimicrobials to veterinary workers for disposal (Table 5).

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Table 5. Practices relating to antimicrobial use in animals.

https://doi.org/10.1371/journal.pgph.0002701.t005

Discussion

This study presents findings on knowledge and perceptions of AMR, as well as practices relating to the use of antimicrobials in humans and animals in a community setting in Wakiso district, Uganda. Despite participants’ good knowledge and perceptions of certain aspects of AMR such as the use of antimicrobials only when prescribed by health professionals, practices on use of antimicrobials in both humans and animals were generally poor. For example, not completing the full course of treatment in humans, poor disposal of expired animal antimicrobials, and using own judgement as a basis for determining the duration between treatment of animals and consumption / selling of their products were established in the study. Our findings offer an understanding of the complexities of antimicrobial use in community settings and present some of the barriers to putting knowledge into action to enhance AMS. This study provides a spotlight on both human and animal health thereby contributing to data on AMR in community settings, an area that is still understudied and misunderstood [23, 31]. Therefore, the study provides evidence of the need for sustainable solutions that consider all aspects of behaviour change to help tackle AMR by promoting a holistic view of AMS among humans and animals using a One Health approach.

Despite many participants in our study earning a meagre average monthly salary of less than 15 USD and (45.2%) of them reported to having sold items or borrowed money in the past in order to access antimicrobials, the majority (71.8%) considered antimicrobials accessible and usually affordable. Communities in districts such as Wakiso that have many private and public health facilities are likely to have greater access to antimicrobials [27]. In our study, participants who were higher income earners were more likely to have completed a given antimicrobial course. Economic status can influence the pattern of antimicrobial use in humans [17]. Indeed, a study on acute respiratory infections (RTIs) in Uganda also reported increased antibiotic usage among households with higher income status [11]. Another possible reason is that higher earners are less likely to worry about the affordability of drugs in the future [16]. High-income earners may also have attained a higher level of education hence literacy that would promote their adherence to public health messaging on medication. On the contrary, people with very low income are always under financial pressure and therefore might not understandably prioritise purchasing full doses of medicine [32], despite understanding the importance of completing the treatment course as stipulated by (67%) of the participants. Evidence on shorter courses of antibiotics, particularly for RTIs favouring lesser days is promising for completeness of dosage [33]. Shorter course length for antimicrobials could therefore be considered whenever feasible to enhance patients completing of the dosage.

Participants who were single were more likely to have completed a given antimicrobial course. This may be because individuals who are single usually stay alone and may have less reason to hold back part of a course of antimicrobials for use by others, in cases where the infection is transmitted to several members of a household. This is in line with the finding from our study that those who had an antimicrobial at home were less likely to complete a given antimicrobial course. This could suggest that, although a full antimicrobial course is prescribed, the recipient might reserve a portion of it at home for future use by themselves or family members [34–36]. Indeed, (72.7%) of participants in our study reported that the main reason for not completing the whole antimicrobial course was the resolution of the symptoms. This finding is similar to studies done in India [37] and Uganda [16] which found that resolution of signs and symptoms was associated with not completing an antimicrobial dose. More education and awareness are needed on the appropriate use of antimicrobials specifically from health professionals to ensure the optimal and intended effects of the use of these medicines.

Participants indicated that antimicrobials from private pharmacies and drug shops nearest to their households were expensive. High healthcare costs especially out-of-pocket expenditure is a major contributor to poor health-seeking behaviours [7, 38, 39]. This could also potentially deter community members from seeking health information from health professionals therefore increasing self-medication practices [14]. Participants indicated that their main source of information about AMR (57.5%) was from their families, friends, and close relatives rather than health professionals. Another study also asserted that a vast proportion of the population in community settings did not seek health information from health professionals [16]. This is supported by the Ministry of Health (Uganda) report which stated that the lack of health information in most cases causes people to self-medicate [15]. In our study, participants who had received advice from a health worker were more likely to complete the course on antimicrobials. This suggests that interventions aimed at promoting AMS should be community centred, with more emphasis on increasing awareness on AMR and its implications on cost-effective treatments in future.

Participants in our study had relatively good knowledge on AMR and how antimicrobials should be used in humans, with a few misconceptions evident. Majority (49.3%) of participants in our study had at least primary education, which could have influenced their knowledge of the appropriate use of antimicrobials. Indeed, the majority of participants were aware that resistant infections may be difficult to treat and could cause problems for them or their families. In addition, many participants agreed that antimicrobials should be used only when prescribed by a health professional. General knowledge about the importance of infection prevention measures such as hand washing (100%), and childhood vaccinations (98.1%) were also high in our study. This is different to previous reports which showed lack of knowledge about the appropriate use of antimicrobials [4, 24, 39]. Contrarily to our study, a recent study in Kasese, Uganda found that 78% of surveyed pastoralists did not know about AMR [40]. This result differs from our study probably because it was carried out in the Western region of the country. It is also possible that earlier interventions in Wakiso district such as the training of community health workers on AMS [30] may have increased community knowledge.

Among participants who kept animals, pigs and poultry were the most prevalent. This finding is similar to other studies in Kampala [41] and Wakiso [12] districts which found that piggery and poultry farming where highly practiced. This finding is not surprising as Uganda’s main economic activity is agriculture including animal husbandry particularly in rural areas [42, 43]. Indeed, it is common for households to have animals for food security and sale in Uganda [42–44]. In our study, few (13.7%) participants reported using antimicrobials to fatten or increase the growth of their animals. This is encouraging and suggests a change in knowledge and resulting behaviours when compared to a previous study conducted earlier which reported 90% of households using antimicrobials as growth promotors [45]. However, prophylactic administration of antimicrobials to animals that were not sick (61.3%) was common in our study. This finding is similar to previous studies where households were using antimicrobials for disease prevention in Uganda [45], Kenya [46] and five other African countries [47]. This calls for interventions to raise awareness on measures to prevent diseases in animals as opposed to relying on antimicrobials. This could be a powerful driver to reduce inappropriate use of antimicrobials in animals among communities [6].

The majority of participants in our study reported obtaining antimicrobials for use in animals from veterinary workers (74.5%) and using them for the duration recommended by the provider (74.5%). In addition, (91.8%) reported that they commonly received advice on the use of antimicrobials in animals from veterinary workers. Similar findings regarding advice on the use of antimicrobials were found in Bangladesh commercial chicken production farmers [48] and pig farmers in Uganda [49]. This finding is different from other studies where advisory input from animal health professionals was rare [45, 47]. More research is needed to ascertain the facilitators of performance among veterinary officers in animal welfare. In addition, since many community members rely on the advice of veterinary workers, AMS efforts should focus on supporting veterinary professionals to promote appropriate alternatives to using antimicrobials for veterinary prophylaxis and growth promotion. This would minimize the inappropriate use of antimicrobials as a result of unqualified and unknowledgeable veterinary officers [45, 48, 50]. Most of the participants in our study who owned animals disposed unwanted antimicrobials, sachets and bottles through burning, throwing them into pit latrines, rubbish pits and open drains, yet inappropriate disposal in the environment is an important driver of AMR. In England, antibiotic amnesty campaigns are being conducted to raise awareness on risks of poor antimicrobial disposal. As part of this campaign, people are encouraged to return of expired and unwanted antibiotics to community pharmacies for safe disposal [51]. We recommend use of a similar campaign in Uganda with a focus on proper disposal of expired and unused animal antimicrobials, and emphasis on raising awareness on the role of the environment in AMR.

Our study took a One Health approach which is a strength particularly in this era when working across disciplines is being encouraged. Another strength of the study is that it focused on knowledge, perceptions and practices relating to antimicrobial use in communities, while the majority of previous studies relating to AMS in Uganda have focused on larger healthcare facilities [52, 53]. However, this study relied on self-reported responses from participants hence the possibility of recall bias, especially for questions that required participants to remember past events. Another limitation is that the study was only carried out in two town councils within Wakiso district, hence the findings may not be applicable to other settings.

Conclusion

Participants were aware of many aspects of AMR and had good perceptions on the need to take steps to avoid infections and seek advice from human and animal health professionals before taking antimicrobials or giving them to animals. However, inappropriate practices such as not completing the prescribed antimicrobial course and using antimicrobials to prevent animals from becoming sick were commonly encountered. Future interventions tackling AMR should take a One Health approach to help address the gaps in knowledge and sub-optimal practice relating to antimicrobial use in humans and animals at community level.

Supporting information

Acknowledgments

We would like to appreciate all members of the broader project team (UK and Uganda), research assistants, community mobilisers, community health workers, local leaders and study participants for their contribution to the study. We also want to thank all stakeholders who supported implementation of the study including: Ministry of Health; Wakiso District Health Office; and Local Council 1 leaders of the different study villages.