Antibiotic Utilization Patterns and perception about antimicrobial resistance among forcibly displaced persons in Uganda, Yemen, and Colombia

doi:10.21203/rs.3.rs-3551532/v1

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Research Article

Antibiotic Utilization Patterns and perception about antimicrobial resistance among forcibly displaced persons in Uganda, Yemen, and Colombia

https://doi.org/10.21203/rs.3.rs-3551532/v1

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Background

Forcibly displaced population are exposed to many socioeconomic determinants, which predispose them to negative health outcomes, like antimicrobial resistant infections (AMR) and inaccessibility to life saving antibiotics. Poor quality antibiotics pose a threat in further driving AMR in these populations. Although there are (inter-)national policies in place to fight AMR there is a gap in recognizing the specific challenges for these people. Our study wanted to investigate the nexus of these global challenges by identifying and analyzing key barriers of access to quality-assured and affordable antimicrobials. Our study sites consisted of three countries that carry a high burden of forced displacement. The study population included South Sudanese refugees in Uganda, internally displaced people (IDPs) in Yemen and Venezuelan migrants in Colombia.

Methods

Semi-structured questionnaires with single-choice, multiple-choice and open-ended questions were used to capture perceptions of displaced populations about access to and quality of antimicrobials, and their knowledge of AMR. Sample size was 36 refugees in Uganda, 50 IDPs in Yemen and 50 migrants in Colombia. Because of the small study sample size, we conducted mainly univariate analysis.

Results

The majority of the 136 participants were female and had no health insurance. Obtaining antibiotics/antimicrobials through informal pathways, either without a doctor's prescription or through family and friends, was common across all study sites. Knowledge of AMR was generally low; usage of antibiotics preventatively or inappropriately was practiced especially in Yemen and Uganda. Barriers to access included mainly financial constraints in Colombia and Uganda, prescription requirements in Yemen and Colombia, reachability of healthcare centers in Yemen as well as nonavailability of drugs in Uganda.

Conclusion

Our multi-centered research identified common barriers to accessing quality antimicrobials among refugees/IDPs/migrants and common use of informal pathways. The results suggest that knowledge gap about AMR may lead to potential misuse of antimicrobials and therefore the rise of AMR within these populations. Possible future interventions designed for similar humanitarian settings should consider these interlinked barriers.

Antimicrobial resistance

Antibiotics

forcibly displaced persons

refugees

access

affordability

availability

Yemen

Uganda

Colombia

Antimicrobial resistance (AMR) is one of most significant global health challenges of our time. Although the development of resistant pathogens thriving to survive is an inherent part of nature, current practices in overuse and misuse of antibiotics(1) have accelerated this process. Between 2000 and 2015, antibiotic consumption has increased by 65%, mainly driven by the economic growth of low- and middle-income countries (LMICs)(2). At the same time, the pipeline of new antibiotics is drying up.(3) Although the drivers of resistance are manifold, one pillar consists of anthropogenic factors, like the often inappropriate and broad use of antibiotics, poor treatment adherence and increased disease transmission through global travel and trade(3). In addition, poor quality or substandard antimicrobials continue to proliferate in low- and middle-income countries(4, 5) and contribute to AMR even when the patients are adherent(6, 7).

Another global challenge of our time is the unprecedented number of people who are forcibly displaced from their homes due to conflict, climate change and economic collapse. The United Nations has called the past ten years the “decade of displacement” and the most recent United Nations High Commissioner for Refugees (UNHCR) numbers show that over 100 million people are currently displaced globally due to conflict and persecution(8), often housed within countries with fragile health systems with inadequate capacity to diagnose, manage and treat life-threatening illnesses(9). Migrants are exposed to many socioeconomic determinants that predispose them to negative health outcomes, including high population concentration in a small area, unavailability of adequate health care and poor sanitary conditions amongst others. These determinants may also increase the risk of disease transmission and act as drivers for AMR(10). Moreover, access to health care services among these populations is challenged with several barriers that include: limited or restricted access to health care services in host settings or countries, language barriers, cultural differences, financial limitations and discrimination(11).

Even with the various global and national policies addressing AMR(12), there is a gap in recognizing the specific challenges that displaced populations face. The necessity for research at the nexus of these two global challenges was recently emphasized in the latest Global Evidence Review on Health and Migration (GEHM) series by the World Health Organization. In their systematic review the authors highlight the significant research and knowledge gaps on access to antibiotics by refugees and migrants in LMICs. Other qualitative studies highlight the importance of informal pathways (such as over the counter pharmacy disposal), as well as research looking into the use of substandard and falsified antibiotics in these settings (13).

Aim

The overall goal of this comparative case study was to identify key barriers of access to quality-assured and affordable antimicrobials for refugees from South Sudan in Uganda, internally displaced populations (IDPs) in Yemen and migrants from Venezuela in Colombia. Furthermore, we aimed to investigate (i) prescription and utilization patterns of antibiotics among refugees/IDPs (ii) their knowledge about AMR among the beneficiary population and (iii) perceptions of the quality of antimicrobials they were prescribed.

Study population selection

Uganda, Yemen and Colombia were chosen because of their relatively high uptake of forcibly displaced persons within their respective continents. Uganda hosts one of the largest displaced populations in Africa, about 1.5 million of refugees mainly from the neighboring South Sudan (65%) and the Democratic Republic of Congo (DRC) (31%). Most of these refugees are housed in settlements alongside the host community across the country(14). The Ugandan Government has a progressive asylum regime and works closely with the UNHCR and national and international organizations to integrate refugees into the Ugandan society. For the health care sector this means that refugees have access to the public health care system and have access to the same health facilities as the host population(15). Yet, Uganda’s main challenge with refugee inclusion and provision of equitable health care is the country’s dependency on financial aid from the UNHCR and other humanitarian aid organizations(14).

Unlike Uganda, most of the forcibly displaced people in Yemen are not refugees from another country, but IDPs who are almost all Yemeni citizens. As of end of 2021, more than 4 million people were estimated to have been forced to flee their homes since the beginning of the conflict in Yemen in 2014(16). Although the majority of IDPs are hosted within communities, it is estimated that more than 1.5 million live in more than 2,300 unplanned and informal settlements(17). IDPs often experience exclusion as a result of challenges related to integration with host communities, areas of origin, education levels, and access to income and to aid. The UNHCR and the International Organization for Migration (IOM), that work alongside other non-governmental organizations (NGOs), are the main providers of services including health services. The protracted conflict has led to an economic crisis, with 81% of Yemenis living below the poverty line as well as a health care crisis with only 50% of public health facilities being operational. This combined with reductions in humanitarian assistance due to funding shortfalls have led to increased levels of vulnerability for those who rely on humanitarian assistance(18).

Colombia’s situation is different from both Uganda and Yemen. Most of the 2.4 million forcibly displaced migrants are Venezuelans who were forced to flee their country, not due to war, but due to economic collapse(19, 20). Furthermore, Colombia also has one of the largest IDPs in the world, with 7.5 million reported in 2016(21). Most of them were forced out of their homes due to the decades long internal conflict in the country. Unlike Uganda or Yemen, there are no camps for displaced people in Colombia, and the displaced population lives alongside the non-displaced local population. Although Colombia has had a plan for Venezuelan migration since 2018, the main problem is posed by the fact that the majority of the migrants in the country without a legal migration status due to reaching Colombia through informal border crossings and the impossibility of obtaining official documents in Venezuela(22). Therefore, most of them are not recognized as refugees by the Colombian state(23). Due to their irregular migration status, Venezuelans can only access health care services in emergencies or for public health interventions, like vaccinations(24).

In response to the challenge of AMR, both Colombia and Uganda have developed National Action Plans (NAPs) and strategies for AMR stewardship(25)^,(26). They have also launched national educational campaigns to improve the understanding of AMR among the general population(27)^,(28). It is, however, unknown what effect, if any, these interventions have had among forcibly displaced populations. Antibiotics are classified as prescription-only medicines in both countries. However, self-medication and over-the-counter sales have been reported as common(29)^, (30). In Yemen, over-the-counter availability of antibiotics is coupled with the lack of coordinated efforts to eliminate inappropriate use of antibiotics(31). Furthermore, the country just recently (at the end of 2022) published a NAP to combat AMR (32). Potential effects of this NAP have still yet to be investigated.

Study design and sample size

The study was a cross-sectional survey using a semi-structured questionnaire for data collection. Data collection took place between February and May of 2021 in all three countries. It comprised multiple choice questions with single-choice and multiple-choice answers as well as open-ended survey questions. To have a more overarching approach the questionnaire is asking about antimicrobials unless the questions focused specifically on antibiotics. We used descriptive statistics to analyze the quantitative data. Responses to open-ended survey questions were categorized using thematic analysis. The questionnaires were primarily composed of validated instruments and questions used in other research studies(11, 33) and the German Health Interview and Examination Survey for Adults (DEGS), a national representative survey that was developed by the German Robert Koch Institute (RKI)(34). In collaboration with our research team members in Uganda, Yemen, and Colombia, the instruments were adapted to forcibly displaced persons in the particular setting of these three countries. The questionnaires were developed in English and translated into Arabic and Spanish by our team members. They can be found in the Supplement Information to this paper. We aimed to include 50 participants for each country population. In Yemen and Colombia, the sample size was reached, while in Uganda 36 refugees answered the questionnaire.

Data collection

In each setting, participants were recruited and surveyed by local team members of our consortium. In Uganda the study was conducted in the Kiryandongo refugee settlement located in Bweyale in Kiryandongo district. Seven public and private health facilities in the settlement and its periphery were targeted (Panyodoli health Centre III, Panyadoli hills health Centre II, Nyakadot health Centre II, Kiryandongo hospital, Lacor allied medical Centre, Juba link medical Centre, Bweyale medical Centre). Systematic sampling of respondents was employed, where every second client exiting each clinic was chosen. In Yemen, the participants were selected from the three most crowded IDP camps in the Dar Sad district of the Aden governorate. In Colombia, migrants were selected from the Kennedy district of the city of Bogotá. Due to social gathering limitations of the Covid-19 pandemic at that time, snowball sampling was performed in Yemen and Colombia in order to reach the necessary sample size. Ethical approval and informed consent from all participants was obtained for all three study sites.

Variables and data analysis

The questionnaires comprised six sections focusing on utilization patterns and quality of medicine (A), treatment adherence and AMR awareness (B), trust in the health care system (C), factors limiting access and on the access to quality-assured (and affordable) antibiotics (D), and patients’ sociodemographic (E) and socioeconomic parameters (F). Participants were asked to rate importance of different limiting factors according to their experience. These factors comprised: “language barriers”, “non-availability of certain medicines”, “financial barriers”, “the medicine I need is a prescription only medicine”, “time to reach the nearest health care center”, “time to reach the nearest pharmacy” and “no trust in the staff at the health care center”. Each factor could be rated on a five-point scale between “no effect at all” and “very large effect” (Page 9 of supplement 1: Patient level questionnaire). A multiple-choice-question asked participants about factors influencing their decision to get medicines. Possible answers were: “quality”, “price”, “distance”, and an open-end answer with “others (please specify)”.

Because of the small study sample size, we conducted mainly univariate analysis and report mainly in percentages and frequencies. Analyses of quantitative data were conducted using IBM SPSS Statistics version (SPSS Inc., Chicago, IL, USA).

Study population

Out of the 136 refugees, IDPs and migrants included in this study the majority was female (27/36, 75.0% in Uganda, 27/50, 54.0% in Yemen and 36/50, 72.0% in Colombia,). Most of the participants answered that they were unemployed (25/36, 75.0% in Uganda, 22/50, 44.0% in Yemen and 26/50, 52% in Colombia) and an overwhelming majority had no health insurance (32/36, 89.0% in Uganda, 50/50, 100.0% in Yemen, and 44/50, 88.0% in Colombia). Information about other sociodemographic characteristics of survey-takers (period of current residency, highest educational level, expenditures) can be found in Table 1.

Table 1

Study population characterization
		Colombia		Yemen		Uganda
Number (n)		50		50		36
		n	%	n	%	(n)	%
Sex	Male	14	28.0%	23	46.0%	9	25.0%
	Female	36	72.0%	27	54.0%	27	75.0%
Age	18–19	3	6.0%	5	10.0%	10	27.8%
	20–29	25	50.0%	13	26.0%	14	38.9%
	30–39	15	30.0%	13	26.0%	8	22.2%
	40–49	4	8.0%	8	16.0%	1	2.8%
	50–59	3	6.0%	6	12.0%	1	2.8%
	60–69	0	0.0%	5	10.0%	0	0.0%
	> 70 and above	0	0.0%	0	0.0%	2	5.6%
Nationality	State Citizen	0	0.0%	50	100.0%	0	0.0%
	Foreign (South Sudan, Venezuelan)	50	100.0%	0	0.0%	36	100.0%
Highest educational level	No schooling	0	0.0%	8	16.0%	5	13.9%
	Primary school	0	0.0%	12	24.0%	22	61.1%
	Incomplete intermediate school	2	0.0%	0	0.0%	0	0.0%
	Intermediate school	0	0.0%	13	26.0%	0	0.0%
	Incomplete secondary school	12	24.0%	0	0.0%	0	0.0%
	Secondary school	16	32.0%	14	28.0%	9	25.0%
	Technical college	5	10.0%	2	4.0%	0	0.0%
	Incomplete university degree	6	12.0%	0	0.0%	0	0.0%
	University degree	9	18.0%	1	2.0%	0	0.0%
Professional status	Not employed	26	52.0%	22	44.0%	25	69.4%
	Part time employed	4	8.0%	12	24.0%	4	11.1%
	Occasionally/irregularly employed	8	16.0%	7	14.0%	4	11.1%
	Full time Employed	4	8.0%	5	10.0%	3	8.3%
	Independent	8	16.0%	0	0.0%	0	0.0%
	Retired	0	0.0%	3	6.0%	0	0.0%
	Vocational training/student	0	0.0%	1	2.0%	0	0.0%
Residency status	Residency permit for 3 years	5	10.0%	All IDPs, therefore not asked		2	5.6%
	Residency permit for 1 year	6	12.0%			0	0.0%
	Permanent residency	4	8.0%			2	5.6%
	No residency title	35	70.0%			26	72.2%
	Other	0	0.0%			6	16.7%
Health Insurance	Yes	6	12.0%	0	0.0%	4	11.0%
	No	44	88.0%	50	100.0%	32	89.0%
Type of residency	Apartment/house	0	0.0%	22	44.0%	10	27.8%
	Temporary accommodation	0	0.0%	20	40.0%	22	61.1%
	Shared apartment	50	100.0%	0	0.0%	1	2.8%
	Communal accommodation	0	0.0%	8	16.0%	2	5.6%
	Other	0	0.0%	0	0.0%	1	2.8%
Place of residency	Rural area	Not asked		0	0.0%	16	44.4%
	Small town (5,000–20,000)			0	0.0%	16	44.4%
	Medium Sized town (20,000–70,000)			50	100.0%	4	11.1%
Period of current residency	Less than 6 Months	15	30.0%	0	0.0%	0	0.0%
	6 Months − 1 year	3	6.0%	0	0.0%	0	0.0%
	Between 1–2 years	8	16.0%	0	0.0%	0	0.0%
	More than 2 years	24	48.0%	0	0.0%	0	0.0%
	3 years	0	0.0%	5	10.0%	3	8.3%
	4 years	0	0.0%	15	30.0%	10	27.8%
	5 years	0	0.0%	15	30.0%	18	50.0%
	> 5 years	0	0.0%	15	30.0%	5	13.9%
Duration lived in current accommodation/house	less than 6 Months	30	60.0%	Not asked		0	0.0%
	< 1 year	8	16.0%			7	19.4%
	1–2 years	8	16.0%			4	11.1%
	More than 2 years	4	8.0%			0	0.0%
	3–5 years	0	0.0%			13	36.1%
	6–10 years	0	0.0%			11	30.6%
	> 10 years	0	0.0%			1	2.8%
Number of rooms (bedroom/dining/kitchen)	< 2	Not asked		14	28.0%	29	80.6%
	2–3			34	68.0%	2	5.6%
	≥ 4			2	4.0%	5	13.9%

Access to affordable and high-quality antimicrobials among the study population through formal and informal pathways

One section of the questionnaire focused on the quality of antimicrobials. When asked, apart from two participants (2/50, 4.0%) in Colombia none of the survey takers knew the producer of the antimicrobial agent across all three study sites. Moreover, in Yemen and Uganda no participant knew the expiration date of the administered antimicrobial. Yet, in Colombia 32/50 (64.0%) of Venezuelan migrants knew the expiration date and out of these 5/34 (14.7%) had received expired antimicrobial within the last year. Despite this fact most participants in Colombia were satisfied with the quality of the used medicine (41/50, 82.0%), followed by Uganda (22/35, 62.86.0%) and Yemen (26/50, 52.0%). There was no way of testing the quality of the used medicine in Yemen and Uganda. Surprisingly, in Colombia 8/50 (16.0%) respondents said that they have a way of testing them.

Regarding the payment of medicine, 45/50 (88.0%) of Venezuelan migrants and 38/50 (76.0%) of Yemenis IDPs paid it out of their own pocket, whereas the response in Uganda was more distributed with 18/36 (50.0%) answering to pay out of their own pocket and 14/36 (41.7%) who were given medicine at a health care facility.

Furthermore, the responses suggest that informal pathways play an important role in obtaining antimicrobials/antibiotics. While 21/36 (58.3%) respondents in Uganda received their medicine through doctors’ prescription, only 14/50 (28.0%) in Colombia and 23/50 (46.0%) in Yemen did. Many participants received their medicines without prescription; 32/50 (64.0%) in Colombia and 17/50 (34.0%) in Yemen, while another 10/50 (20.0%) of Yemeni IDPs were given their medicine by a relative or friend (Fig. 1A). In the follow up question asking how the patients would receive antibiotics if they did not have a doctor’s prescription, 39/50 (78.0%) in Colombia, 32/50 (64.0%) in Yemen, and 23/36 (63.9%) in Uganda answered that they would get them from a pharmacy. This was followed by family members in Yemen (10/50, 20.0%) and Uganda (8/22, 22.2%). Overall, participants reported sharing their antibiotics with friends and/or family members; 26/50 (52.0%) in Colombia, 24/50 (48.0%) in Yemen, and 18/36 (50.0%) in Uganda (Fig. 1B).

Moreover, distrust in the health care system was a concern in Colombia. 36/50 (72.0%) of participants believed that there is a hostile behavior of health care workers towards migrants and almost half of them think that they receive lower quality of health care due to their migrant status (24/50, 48.0%). 21/50 (42.0%) of Venezuelan respondents felt that they have no power in decisions related to their health.

Decision about getting medicines were reportedly, in Colombia 36/50 (72.0%) answered that price influences their decision the most, followed by its “quality” (32/60, 64.0%). In Yemen 25/50 (50.0%) mentioned "quality and price”, followed by “price” alone 13/60 (26.0%). For Ugandan refugees’ “price” was by far the most influential factor (17/36, 47.2%), while about a quarter of participants mentioned that “distance” (8/36, 22.2%) and “quality” (9/36, 25.0%) were influential factors.

Barriers to accessing medicine and healthcare among the study population

In Yemen surveyed IDPs reported that the “time to reach the nearest health care center” (13/50, 26.0% “mainly large effect” or “very large effect”) and “the used medicine needs prescription” (12/50 24.0% “mainly large effect” or “very large effect”) were the top barriers in accessing quality-assured antimicrobials. While in Uganda the top two barriers were the financial barrier (23/36, 63.9%“very large effect” or “mainly large effect”) and the unavailability of certain medicine (19/36, 52.8% “very large effect” or “mainly large effect”), the main access limiting factors in Columbia were 1.) financial barriers (26/50, 52.0% “very large effect” or “mainly large effect”) and 2.) that the used medicines needed prescription (17/50, 34.0% “very large effect” or “mainly large effect”). The complete response distribution to this section can be found in Fig. 2.

Appropriate use and misuse of antimicrobials within the study population

Among the participants the 30-day prevalence of using at least one antimicrobial agent differed in the three study sites: While only 13/50 (26.0%) of Venezuelans had taken antimicrobials 30 days prior to the study, the number was higher in Yemen (42/50, 84.0%) and in Uganda (22/36, 61.1%).

Awareness about antimicrobial resistance was low among the participants in all three study sites (see Fig. 3A), nonetheless differed between the countries. Participants reported taking antibiotics to prevent a cold; 18/36 (50.0%) in Uganda and 21/50 (42.0%) in Yemen. Also, 26/36 (72.2%) of respondents in Uganda said that they are taking antibiotics when they have a cold. In Yemen the response rate was similar (32/50, 64.0%). When asked if they would “stop taking antibiotics when they feel worse” (11/50, 22.0% in Yemen and 16/36, 44.4% in Uganda) and “stop taking antibiotics when feel better” (15/50, 30.0% Yemen and 11/36, 30.6% in Uganda) both groups showed similar results. Contrasting both countries, responses from Venezuelan migrants differed on these questions: only 5/50 (10.0%) took antibiotics to prevent a cold, 16/50 (32.0%) used antibiotics to treat a cold and 34/50 (68.0%) stopped treatment when they felt better. Overall, across all countries most participants adhered to the treatment instructions by taking the medicine for the whole duration of the prescribed period (Fig. 3B).

To the best of our knowledge, this is the first multi-country study to investigate the prescription and utilization patterns of antibiotics/antimicrobials and assess the knowledge about AMR and the perception of the quality of antibiotics/antimicrobials among forcibly displaced communities (refugees/IDPs/migrants) in the three LMICs, Uganda, Yemen and Colombia. The access to high-quality and affordable antibiotics is not only important to battle AMR, but the provision of essential drugs, like antibiotics, is also a basic human right under international law (35). Therefore, it is of utmost importance to ensure that a high-quality standard is met. This accounts especially for vulnerable populations, like refugees and IDPs. The latest GEHM Report by the WHO confirmed our stance on the necessity of research into AMR among refugees, IDPs and migrants in LMICs. Due to the small sample size of our study population, we refrained from disaggregating our results by gender as recommended by the The Sex and Gender Equity in Research (SAGER) guidelines.

Intercountry variation in access to quality antimicrobials

The results of our study suggest that challenges in the access to quality antimicrobials are similar across all three study sites. The decision to buy an antibiotic/antimicrobial is mostly influenced by its price, followed by its quality. In Yemen and Uganda, the payment of antimicrobials was perceived as the biggest barrier to the participants.

Yet, our study showed that there are some intercountry variations specific to contextual problems of each country. In Yemen we identified that the time to reach the nearest health care center was the biggest issue for the surveyed IDPs. This comes as no surprise since the Yemenite health care system has been struggling due to the years long still ongoing civil war. In 2021, the year our study took place, the international committee of the red cross reported that an estimated 20 million people in Yemen lacked access to basic health care with only 51.0% of health facilities across the country still functioning (36). In order to combat this issue international health care organizations like the international medical corps have implemented mobile health care centers in order to provide for essential medical needs (37).

In Uganda on the other hand, participants ranked the unavailability of certain antimicrobials as the second most influential barrier of access. This factor was ranked much lower in Yemen (15/50, 30.0% no effect, 24/50, 48.0% some effect) and Colombia (37/50, 74.0% it had no effect at all and 7/50, 14.0% mainly no effect). This is not a unique problem to the Kiryandongo district but has been reported in other Ugandan districts as well. A study from 2021 showed that in a refugee settlement in the Yumbe District, on average 32% of antibiotics were not available on a given day, and frequently out of stock at health care facilities (38). Challenges in health care supply chains like ineffective coordination and management, inadequate funding and weak regulatory and governance structures at national and sub-national levels have been reported as possible causes for this issue(39).

In Colombia and Yemen, participants reported that the necessity of prescription of antimicrobials was the second most influential barrier of access. Prescription of antibiotics/antimicrobials is important to ensure regulated, high-quality medicine. But inadequately equipped (Uganda) or hard to reach (Yemen) health care facilities and no integration in the public health insurance system (Colombia) combined with a knowledge gap about AMR among forcibly displaced persons could drive them to access antimicrobials through informal pathways. Additionally, the lack of confidence in the quality of available medicines could also drive doctors or patients to prescribe or use multiple antibiotics, or follow more aggressive antimicrobial treatment regimens (40). Therefore, it is crucial to consider the quality of antibiotics/antimicrobials available in the market while discussing questions about their rational use.

Access of antibiotics through informal pathways

Although regulations (like NAPs) and policies (only prescription antibiotics) are in place, there is a gap between policies and the actual situation on the ground. As shown above, informal pathways, like pharmacies dispensing antibiotics/antimicrobials without prescription, played an important access point to health care across all three study sites. The importance of these access points must be recognized, and pharmacists should be better educated about AMR and antibiotic prescription patterns. Furthermore, the majority of migrants in Colombia and IDPs in Yemen reported having paid for their medicine out of pocket. Similarly, in Uganda, half of the study participants reported to pay on their own. Making essential medicines, like antibiotics, free of charge and dispensing them at certified healthcare sites could have a positive effect in three ways: firstly, the quality of the dispensed medicine could be monitored. Secondly, the beneficiary population would interact with health care professionals directly. They could then monitor their health status and decide if a certain antibiotic is necessary and/or effective. And thirdly, this could aid to build trust in the local health care systems (again) and could potentially lead to less utilization of informal pathways. Of course, different country specific contexts must be taken into account: As mentioned above “time to reach the nearest health care center” was an influential challenge in Yemenis IDPs. In Uganda less than half of Sudanese refugees have also ranked this factor to have a “very large” or “large” effect on the access to quality antimicrobials. Therefore, the proposed dispensatories would have no effect if they are unreachable. A possible solution could be mobile health care sites that attend to patients in their homes. This a well-received practice that has already been implemented in certain locations, like parts of Yemen (as mentioned above) as well as in Syria and Palestine by the United Nations Relief and Works Agency for Palestine Refugees in the Near East (UNRWA)(41).

Knowledge gap leads to misuse of antibiotics

Awareness about AMR was low across all study sites. This lack of knowledge manifests itself in treatment adherence patterns of said population like taking antibiotics to prevent a cold. Nowadays it is known in the medical field that most colds and coughs are caused by viral infections, for which antibiotics show no effect. On the contrary, the overuse and abuse of antibiotics is a driver for antibiotic resistance(42). Therefore, combatting the overuse of antibiotics was also adapted as one of the main objectives of WHO Global Action Plan on Antimicrobial Resistance, which was released in 2015(43). Moreover, 68% of participants in Colombia said that they are stopping their course of treatment, when they feel better. Other studies have shown similar results when surveying migrants: In Australia almost 70% of participating Chinese migrants said they would stop their course of treatment once they started feeling better(44). Additionally, physicians in Germany and the Netherlands perceived treatment discontinuation due to “feeling better” as a major challenge; they stated in interviews that migrant patients frequently discontinued antibiotic courses when they were free of symptoms(45). Although the scientific opinion about completing an antibiotic course for the whole period is slowly deviating and short-course antibiotics for common infections do not show inferior results(46), the problem about not completing a course might be the misuse of antibiotics by the patients afterwards. They are at risk to keep the antibiotics and self-prescribe them when faced with a similar ailment(47) or share them with friends/family. Our study showed that across all countries sharing antibiotics with family members or friends was a common practice. One of the main objectives of the WHO Global Action Plan of 2015, that is to say the improvement of “awareness and understanding of AMR through effective communication, education and training”(43). Targeted interventions are likely needed for improving AMR awareness and appropriate use of antibiotics among displaced populations.

A solution to this problem could be digital interventions, like mobile applications. In recent years, with the help of Artificial Intelligence, mobile applications have been developed to mainly support healthcare workers in region with lack of qualified personnel(48). But mobile applications targeting patients directly are scarce. They could inform patients not only about AMR and best practices of antibiotic use but could also guide them to the nearest qualified health care center or get them in contact with a health care professional in proximity.

Strengths and limitations

This study has a number of strengths. First, our research team included researchers from the three countries, Colombia, Uganda, and Yemen. This was helpful in ensuring that our investigation was well-adapted to the culture of the target population. Second, our study covered different forced migration scenarios (internally displacement, cross-border forced migration) in three different continents. Third, our study has identified challenges and barriers that limit forcibly displaced populations to accessing quality assured antibiotics/antimicrobials, laying the ground for further research into the development and implementation of interventions.

There are however several limitations. First, we used non-random sampling due to the lack of a sample frames in the three countries. This can affect the possibility of the representativeness of our results to the forcibly displaced populations in the three countries. The lack of sampling frames is a common challenge facing research studies among in the context of forced migration and healthcare (49). To enhance the likelihood of our sample being representative, we recruited a diverse group of participants in terms of age and sex. Second, not all questions of the questionnaire were answered equally across the three study sites. One example being that section C (Trust in the health care system) was only answered in Colombia. Therefore, comparative cross-sectional analysis was not possible for all parts of the questionnaire. Third, the sample recruited for this study was rather small. This was related to the limited time and resources, but also due to the challenges of conducting interviews during the Covid-19 pandemic.

Assessing behavioral, organizational, and social barriers to access to quality antimicrobials, this study sheds some light into the situation of refugees, IDPs and migrants regarding their perception of top barriers of access. Affordability and accessibility of antimicrobials from regulated health care sites remain a challenge across the study countries. Furthermore, we identified antibiotic utilization patterns of refugees and IDPs and found knowledge gaps regarding AMR, which may have led to antibiotic misuse among the study population, like using antibiotics to prevent or treat a cold. Also, we were able to shed a light on this topic in the South American context, which has been underrepresented in research. Lastly, of concern is the use informal pathways by refugees to access antibiotics, such as over the counter sales of pharmacies. Training for pharmacists on drivers of AMR and (mis-)use of antibiotics could be a possible approach to improve the rational use of antimicrobials in these settings. Our study calls for interventions that take into account the complex and interlinked barriers to accessing antimicrobials in humanitarian settings.

AMR Antimicrobial Resistance

DEGS German Health Interview and Examination Survey for Adults

DRC Democratic Republic of Congo

GEHM Global Evidence Review on Health and Migration

LMICs Low- and Middle-Income Countries

IDPs internally displaced populations

IOM International Organization for Migration

NAPs National Action Plans

NGOs Non-governmental organizations

UNHCR United Nations High Commissioner for Refugees

UNRWA United Nations Relief and Works Agency for Palestine Refugees in the Near East

RKI Robert Koch Institute

Ethics Approval

The study was approved by the ethics committee of the University of Aden (Protocol Code: REC-81-2020, Date of approval: 9th August 2020), the ethics committee of the Universidad de Los Andes (Protocol Code 1322, Date of approval: 14th of April 2021) and the ethics committee of the Makerere University School of Public Health (Protocol Code: 0772511444, Date of Approval: 3rd of May 2021).

Consent for publication

Not applicable.

Availability of data and materials

All data generated or analysed during this study are included in this published article [and its supplementary information files].

Competing Interest

The authors declare no competing interest in this research.

Funding

This work was funded by the Volkswagen Foundation (Az.: 9A 548).

Acknowledgments

The authors thank every migrant/refugee/IDP who helped and participated in this study. We thank every researcher who helped in validating and enacting the questionnaire for this study. Furthermore, we would like to thank Prof. Veronika Wirtz and Dr. Hannelore Meyer for their general supervision and valuable advice.

Contributions

DKH is responsible for the study conceptualization, design, data analysis and drafting of the manuscript. SA, PS and CC contributed to the study conceptualization, design, manuscript review and editing. HK, DH, JSPR, JOC, SO contributed to the data collection, data analysis, manuscript review and editing. CPdC, MZ, CGO, OBA and HB contributed to manuscript review and editing. All authors read and approved the final manuscript.

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No competing interests reported.

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Antibiotic Utilization Patterns and perception about antimicrobial resistance among forcibly displaced persons in Uganda, Yemen, and Colombia

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Abstract

Background

Methods

Results

Conclusion

Figures

INTRODUCTION

METHODOLOGY

Aim

Study population selection

Study design and sample size

Data collection

Variables and data analysis

RESULTS

Study population

Access to affordable and high-quality antimicrobials among the study population through formal and informal pathways

Barriers to accessing medicine and healthcare among the study population

Appropriate use and misuse of antimicrobials within the study population

DISCUSSION

Intercountry variation in access to quality antimicrobials

Access of antibiotics through informal pathways

Knowledge gap leads to misuse of antibiotics

Strengths and limitations

CONCLUSION

Abbreviations

Declarations

References

Additional Declarations

Supplementary Files

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