Primary review question.

What is known from existing literature about gender differences in antibiotic use in Southeast Asia?

Secondary review questions.

1. What gender differences in antibiotic use exist across Southeast Asia?
2. What models exist to examine the role of gender in antibiotic use in Southeast Asia?

Eligibility criteria.

Relevant elements of the population, concepts and context (PCC) framework were applied to the research question to identify key terms [12]. The population element was not relevant for this scoping review as this review did not focus on a specific cohort or condition. The core concept examined in this review is antibiotic use. This includes antibiotic use in humans, animals and plants in order to ensure application of a One Health lens. Also, this review only included studies that examined gender in the context of antibiotic use. Studies that either focus on all genders or a specific gender were included in this review. The scoping review only included studies within the context of Southeast Asia to ensure relevancy of the information to Vietnam. The PCC framework used to inform the search strategy is presented in Table 1.

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Table 1. PCC framework for search strategy development.

https://doi.org/10.1371/journal.pone.0259069.t001

A pilot search was conducted in MEDLINE and PubMed databases to identify articles on the topic. The identified key terms were combined to develop the search phrases used for the pilot search. Search phrases included “gender AND antibiotic use”, “gender AND antibiotic use AND Southeast Asia” and “antibiotic use AND Southeast Asia”. The text words contained in the titles and abstracts of relevant articles were examined to identify synonyms for the key terms. An additional search was then conducted in PubMed to identify Medical Subject Headings (MESH).

The final searches were as follows: “gender AND antibiotic use AND Southeast Asia” and “gender AND antibiotic use OR antibiotic resistance OR knowledge AND attitudes AND practice AND Southeast Asia.”

Searches were also conducted using the following phrases and terminology for each of the countries in the region of interest, more specifically, member countries of the Association of Southeast Asian Nations (ASEAN), as follows: “gender AND antibiotic use AND Vietnam,” “gender AND antibiotic use AND Malaysia,” and “gender AND antibiotic use AND Thailand,” to name a few. However, due to the limited number of relevant search results, the search was widened to be “gender AND antibiotic use AND Southeast Asia.”

Similarly, searches were conducted using the following phrases “gender AND antibiotic use OR antibiotic resistance OR AMR OR knowledge AND attitudes AND practice AND Vietnam, etc.” for each of the ASEAN countries. This search was also widened to include Southeast Asia due to the limited number of relevant results that appeared when each specific country was used in the search. Moreover, a separate search was conducted by replacing the term “antibiotic resistance” with “AMR.” In PubMed, it was found that both searches yielded the same results. However, in ProQuest and Semantic Scholar, using the term “antibiotic resistance” yielded more results, including the results from the use of the term “AMR,” and thus, antibiotic resistance was used in the final search strategy to widen the results.

Inclusion criteria.

The review only included articles that were: (i) peer-reviewed journal articles; (ii) published in English; (iii) published in the last ten years (from 2011 to 2021); and (iv) focused on Southeast Asia.

Only peer reviewed articles were included to ensure validity of the findings. In addition, articles published in the last ten years were of focus to ensure relevancy to current antibiotic use practices and AMR surveillance strategies. Articles that either focused on Southeast Asia as a whole or specific countries within the region were included. More specifically, only articles on member countries of ASEAN, namely Brunei Darussalam, Cambodia, Indonesia, Lao PDR, Malaysia, Myanmar, Philippines, Singapore, Thailand and Vietnam [13], were of interest as findings from these countries would be of most relevance to the context of Vietnam.

Exclusion criteria.

Articles focusing only on healthcare settings such as clinics or hospitals were excluded as this review focuses on antibiotic use in the community. Although antibiotic use in healthcare settings also influences AMR, research examining antibiotic use in community settings is scarcer. There is a need to examine use in community settings to develop a better understanding of what influences antibiotic use behaviour, especially use without consultation at healthcare settings. Thus, this review aimed to inform this gap in research and specifically map out articles that examine gender differences in antibiotic use in the community setting. Identifying root causes to inappropriate use at the community level will also inform practice in healthcare settings as well. Moreover, articles examining gender in the context of antibiotic prescription were excluded. This was because preliminary investigation of the topic indicated that articles examining differences in gender and prescribing patterns focused on primary care settings and prescribing behaviour of healthcare professionals as opposed to antibiotic use behaviour among the general public.

Knowledge of antibiotics and AMR in humans.

Results on gender differences in knowledge of antibiotics varied by context. However, generally, in studies examining antibiotic use in humans, females were found to have better knowledge of antibiotics and AMR in comparison to males. Some studies indicated that males had lower levels of knowledge, were more likely to believe that antibiotics could be used to treat viral infections and that adherence was not required once symptoms disappeared [14, 15, 22]. This was attributed to females being more likely to seek help and visit healthcare facilities, thus receiving more information on antibiotics [3, 15]. One study in particularly stated that women with higher levels of education and of higher socioeconomic status had 1.18 times higher chance of obtaining information on appropriate use of antibiotics and AMR in comparison to males [18]. A study among children in primary school examining knowledge of efficacy of medicines (including antibiotics) also found that young girls were more aware of the efficacy of medicine than boys and attributed this to girls having a greater tendency to obtain information from healthcare professionals [15]. When examining the roles of fathers and mothers in caring for children, results indicated that although fathers used antibiotics to treat symptoms such as coughs, mothers had greater knowledge of antibiotics due to being the primary caregivers and thus, having better health-seeking behaviour [17].

Knowledge of antibiotics and AMR in animals and plants.

On the contrary, a study conducted among small-scale pig farms in Cambodia found that 74% of male farmers had heard of AMR in comparison to 39% of females. This was attributed to males having higher levels of education and being held responsible for treating sick pigs, thus resulting in more experience with antibiotics [5]. Similarly, a study examining awareness of prescription medicines including antibiotics also indicated that females had lower knowledge than males [21]. This was particularly found to be true among females who had lower levels of education, lower income, belonged to ethnic minority groups and worked in agriculture, fishery, or forestry [21].

When examining knowledge of antibiotic use and AMR in terms of environmental impact, one study on livestock and aquaculture producers found that a majority of producers agreed that AMR has a negative impact on the environment. However, differences in knowledge on this topic between genders was not examined [19].

Thus, although a greater number of studies included in this review indicated that females generally had greater knowledge of antibiotics in comparison to males, this was primarily true when examining antibiotic use in humans. Findings from articles on gender differences in knowledge of antibiotic use in animals and plants, however, contradicted this and found that males had greater knowledge. Thus, the relation between gender and knowledge of antibiotics remains unclear. This is due to knowledge on antibiotics being heavily related to gender norms and roles that exist within the community and thus varying between communities. Thus, there is a need to develop a clear understanding of contextual factors such as gender norms and roles that exist within a community of interest and how these factors influence knowledge of antibiotics and AMR prior to development and implementation of interventions to reduce inappropriate antibiotic use.

Practices related to antibiotic use in humans.

Higher levels of knowledge were found to be associated with better practices related to antibiotic use [19, 20]. Males who had not heard of AMR were more likely to use leftovers or not complete an entire course of antibiotics [3, 14]. This was found to be particularly true among males with lower levels of education [14]. Adherence to antibiotic treatment was attributed to better health-seeking behaviour of females, making them more likely to receive counselling on medication from healthcare practitioners and thus, more compliant [3].

A review examining self-medication practices across Southeast Asia found that there were also higher levels of self-medication with antibiotics among males in comparison to females [10]. However, reasons attributing to the greater prevalence of such behaviour among males were not explored or discussed [10].

One study specifically focused on sexual orientation and examined the behaviour of men who have sex with men with regards to obtaining a prescription prior to taking antibiotics. This study found that men who have sex with men were less likely to seek healthcare services and get a prescription. This may be due to stigma associated with sexual orientation, a lack of trust in confidentiality being maintained by healthcare providers, and a crowded healthcare system [16].

Practices related to antibiotic use in animals and plants.

With regards to antibiotic use in animals, antibiotics were highly used for prophylactic purposes as opposed to for treatment, thus resulting in increased risk of resistance [1]. Females were found to have better practices related to antibiotic use in animals in both studies on this topic included in this review [1, 19]. Reasons for this, however, were not explored in the studies. None of the included studies examined gender differences in practices related to antibiotic use in plants.

Similar to studies examining knowledge of antibiotics and AMR, there were inconsistencies among the findings of studies examining antibiotic use practices in humans, animals and plants. Although most studies indicated that females had better practices related to antibiotic use, one study found that despite males having lower knowledge of antibiotic use and resistance, females were more prone to self-medicate [22]. Moreover, a study which particularly focused on antibiotic misconceptions and non-medical access at the community level found no association between gender and self-medication with antibiotics. Nonetheless, it is important to note that the authors of this study stated that their findings were contrary to previously conducted research which indicated that being female was associated with self-medication with antibiotics [20].

Overall, when examining the role of gender in knowledge and practices related to antibiotics, it is evident that further exploration of reasons for gender differences in these areas is required. Findings on these topics are scarce and appear to vary by context. In addition, gender was often discussed in intersection with other sociodemographic characteristics, particularly level of education and socioeconomic status. Level of education and socioeconomic status were the most commonly used criteria for sociodemographic characteristics in the included studies from different countries across Southeast Asia. Thus, further analysis of the influence of gender on antibiotic knowledge and use, and the intersectionality of gender with other sociodemographic factors that influence inappropriate antibiotic use, must be examined carefully in order to strengthen AMR surveillance strategies at the local and national levels.

Educational interventions.

Although findings on knowledge of males and females were not consistent among the articles included in this review, generally a need to improve knowledge on antibiotic use and AMR among the general public was identified [1, 14, 15]. Improved knowledge will in turn promote better practices related to antibiotics, thus mitigating risk of resistance in humans, animals and the environment. As levels of existing knowledge and current practices vary by gender, there is a need for educational interventions to be targeted and designed with a good understanding of how gender norms and roles in the community influence antibiotic use. For instance, if females are seen as the primary caregivers in a specific community and responsible for treating family members when ill, or in the case of farms, sick animals, identifying females as entry points to improving antibiotic use in this community and creating messages in a manner relatable to their roles in the community will prove to be effective.

These interventions need to focus not just on raising awareness of antibiotic use but also AMR as well [3, 18] with the aim that greater understanding of AMR and its consequences will reduce inappropriate practices such as non-adherence, use of antibiotics as prophylactics and growth promoters, antibiotic sharing and self-medication. Farmers should specifically be trained on appropriate administration of antibiotics to animals and the impact of high levels of antibiotic residue in animals for consumption on humans as well as pathways for transmission of resistance [1].

As the main source of antibiotics was found to be pharmacies, pharmacists play a key role in educating the general public [3, 10]. In addition, healthcare professionals should be actively involved in the development of educational interventions to promote health-seeking behaviour and better antibiotic use practices among the public [15, 22]. Studies also indicated that information on antibiotic use and AMR should be integrated into school curricula as misconceptions on efficacy of medicine exist even among school children and vary by gender [14, 15]. Raising awareness at a younger age could result in promotion of good practices related to antibiotic use early, thus reducing the risk of resistance.

Targeted educational interventions aimed at reducing inappropriate antibiotic use specifically in animals should provide information on animal healthcare, specific approaches to treating different animals such as livestock and aquaculture, the effects of inappropriate use pertaining to the specific animals and how inappropriate use can be avoided [19]. This is especially important as the approaches for care and use of antibiotics vary by animal [19]. A study conducted in Vietnam examining knowledge, attitude and practices of livestock and aquaculture producers regarding antibiotic use and AMR not only found gender differences in antibiotic use, but also found significant differences in knowledge, attitudes and practices between pig producers, poultry producers and aquaculture producers [19]. This further emphasizes the need for educational campaigns to be targeted to the different types of producers with context-specific information pertaining to different animals [19].

Further qualitative research.

Targeted interventions require in-depth understanding of factors that influence knowledge and use of antibiotics among males and females. As research on gender and antibiotic use is limited, and research exploring reasons for gender differences in knowledge and practices related to antibiotics even more scare, there is a need for further qualitative research to develop a greater understanding of differences in knowledge and practices between genders and underlying reasons for these differences. For instance, when exploring the behaviour of farmers in the Mekong Delta of Vietnam, it was found the female farmers were less likely to use antibiotics, however explanations for this behaviour were not explored [1]. To promote appropriate antibiotic use, reasons for such differences in behaviour need to be identified and addressed. Moreover, as these factors are context specific and often intersect with other sociodemographic characteristics, there is a need for further qualitative research within the communities of interest when developing interventions. It is important to note that such qualitative research should be conducted to complement quantitative research aimed at identifying existing knowledge, attitudes and practices related to antibiotic use and effects of misuse [15]. Conducting gender analysis research prior to developing interventions and continuously assessing the impact of the interventions by gender will be beneficial and improve the effectiveness of strategies to reduce the impact of resistant bacteria.

Other recommendations.

Inappropriate use of antibiotics through practices such as self-medication are found to be associated with factors such as inaccessibility, unregulated distribution of medicines and lack of medical professionals and quality healthcare facilities, to name a few [10]. Efforts must be taken at all levels to prevent such inappropriate practices [10]. Governments across ASEAN have developed national action plans to monitor and regulate the use of antibiotics [6, 19]. Despite the existence of such national action plans, there remains a need to further strengthen existing policies in order to effectively monitor and regulate antibiotic use [6]. Indicators measuring factors such as equity and accountability are not the same across countries in the region [6, 19]. For instance, although it is recommended that gender and socioeconomic considerations be made when promoting equity with regards to AMR, not all countries in ASEAN include socioeconomic considerations in their action plans and none of the countries have included gender considerations [6]. Reliable indicators on antibiotic use and AMR in agriculture is particularly limited across the region despite the large use of antimicrobials in this sector [19]. Having regional indicators to monitor and regulate AMR in addition to context-specific indicators will prove to be beneficial in tackling AMR through a One Health approach.

Inappropriate use of antibiotics results in increased risk of mistreatment, adverse drug reactions and resistance [10]. These factors along with the higher burden of infectious diseases in Southeast Asia put healthcare systems in the region more at risk of financial strain [10]. The establishment and enforcement of laws and regulations aimed at ensuring appropriate dispensing of antibiotics through pharmacies as well as increasing awareness of the adverse effects of inappropriate use, quality of antibiotics and promoting health-seeking behaviour can mitigate the risk of AMR [10].

In addition, the high costs associated with hospital treatment affects health-seeking behaviour [17], thus resulting in people opting to use low cost and easily available antibiotics such as amoxicillin [10]. A study conducted examining father’s roles in healthcare seeking for their children found that providing more flexible and affordable options for payment improved health-seeking behaviour as was the case with traditional healers in the Philippines [17]. Implementing regulations to improve affordability of healthcare and provide flexible payment options could result in reduced inappropriate use of antibiotics and promote health-seeking behaviour as well.

A study examining the effects of self-medication with antibiotics across Southeast Asia highlighted the need for organizations at the regional level such as the World Health Organization (WHO), the South Asian Association for Regional Cooperation (SAARC), the Association of Southeast Asian Nations (ASEAN), and the Ministry of Health of countries in the region to work together in the development of interventions targeting common inappropriate use practices across the region [10].

Furthermore, although efforts are being made to reduce inappropriate use and monitor AMR, these efforts focus primarily on human health [19]. There is a need for more data and regulations focusing antibiotic use and resistance in animals and the environment [19]. The national action plans of all ASEAN countries emphasize the importance of One Health engagement, in other words engagement of stakeholders at all levels (decision-makers, regulatory authorities, medical practitioners, veterinarians, pharmacists, etc.) and across human, animal and environmental health sectors, in order to effectively tackle AMR [6]. However, efforts focusing on animal health were found to be scarce, with those aimed at environmental health even more limited [6, 19]. Thus, there is a need to strengthen multisectoral efforts in order to reduce inappropriate antibiotic use in human, environmental and animal health and tackle AMR across nations.

When examining laws and regulations, it is especially important to examine the availability and use of over-the-counter antibiotics as well as the quality of antibiotics. Antibiotics are found to be readily available in local shops across Southeast Asia, as was evident in the study examining the role of roadside (sari-sari) stands in antibiotic distribution in the Philippines [20]. Sari-sari stands are small businesses commonly found in residential areas and observation of these stands indicated that many of them carried and distributed antibiotics that were expired or did not contain an expiration date, thus posing health concerns due to poor quality of these medicines [20]. Interventions at the national as well as the local level are needed to regulate the distribution of antibiotics and particularly reduce the distribution of low-quality antibiotics in countries across Southeast Asia [20]. The quality of antibiotics was usually discussed in terms of purchase without prescription as opposed to the quality of prescribed antibiotics in the included studies. However, the need for people to be aware of quality and check details of the antibiotics they purchase was recommended.

Similarly, when examining antibiotic use among animals in Vietnam, legal antibiotics were often found in livestock feed along with illegal drugs [19]. Removal of antibiotics in commercial feed products is required to combat AMR in animals [19]. In addition, antibiotics were also found to be commonly used for prophylactic reasons and as growth promoters [19]. This inappropriate use of antibiotics in animals may be attributed to the availability of over-the-counter antibiotics and limited supervision by veterinarians, thus resulting in antibiotic residue in meat products which in turn could affect human health and the environment [19]. A Law on Animal Husbandry was developed by the Vietnamese government in order to tackle AMR and antibiotic residues in livestock. However, regulation has proven to be difficult, particularly among smallholder farms, thus emphasizing the need for more regulation of such antibiotic use in animals [19].

In addition to laws and regulations promoting management of quality antibiotics, rewarding responsible prescription and distribution at the community level will prove to be effective in tackling inappropriate antibiotic use and AMR at the community level [19].