Impact of Legislation on Antibiotic Use and Awareness of Beekeepers

Antibiotic use ranged from two to four percent in the three geographical areas, with the EU and US reporting the highest percentages (4%), however with no statistical difference between the EU and US or UK (2%). Respondents in the UK were less likely to use ABs without following label instructions, but the difference was not significant. Reports pertaining to the diseases treated with ABs showed that use against Nosema was significantly higher among US beekeepers (p=.0095) and European Foulbrood (p=.0045) compared to that of the EU (Fig. 1 & 2).

EU beekeepers primarily purchased antibiotics from pharmacies compared to the US where beekeepers acquired ABs from agro-chemical supply shops or the internet, and the UK where beekeepers resorted to national bee inspectors. All three were likely to purchase from veterinarians with no statistical difference between areas (5–11%).

A lack of significance showed accordance among all three geographical areas, indicating ABs were primarily used to treat infections instead of prevention. Moreover, in all areas, between 60–65% of respondents stated the necessity of a prescription to purchase antibiotics.

In a self-identifying knowledge score, all three regions reported having little or some knowledge pertaining to AB issues, with UK respondents reporting significantly less knowledge (p=.013) (Fig. 4). When investigating the function of ABs, the US beekeepers reported believing ABs are medicines that prevent diseases (p=.003) (Fig. 3). The UK beekeepers were more aware of ABs being used to target bacteria compared to the EU, which presented the lowest average response rate. When asked where information regarding ABs was found, EU respondents were statistically more likely to obtain information from veterinarians or other beekeepers compared to both the US and the UK (p=.031; p=.0022), but also the least likely to obtain the information from a beekeeper association (p=.0017; p=.0003). US respondents were more likely to obtain information from books, the internet (p=.0009) and extension services (p=.00001). UK respondents reported using national bee inspectors (p=.0035).

Experience in recognizing bee resistance to medicines was significantly higher for the EU compared to the UK (p=.03) and US (p=.016) (Fig. 5). US responders indicated being more likely to witness AB failure in treating honeybees, although the difference was not significant. UK respondents were also less informed regarding AB residues compared to EU respondents. Responders from all three regions agreed that products deriving from AB treated hives should not be consumed. Beekeepers also believed antibiotic resistance would have a strong impact on their personal lives and hives. Both questions yielded no statistical difference among geographical areas.

Compliance was assessed by asking beekeepers if antibiotics had been used over the past two years, and respondents in all three regions indicated a use ranging from 2 to 4%, with no statistical difference across regions. These findings are likely a conservative estimate, given that beekeepers would be unlikely to admit to unsanctioned AB use. This is further supported by the numerous studies that have exposed frequently detected residues in honey samples, indicating antibiotic use among EU member states (Al-Waili et al., 2012; Reybroek et al., 2012; Galarini et al., 2015; Reybroek, 2017). Al-Waili et al. (2012) reported that 1.7% out of 3855 tested honey samples were noncompliant with current EU standards based on the detection of seven different antibiotic residues. It is not always possible to discern the source of contamination, whether from explicit AB use, honey admixture or environmental pollutants, which makes the current findings so significant (Lodesani & Costa, 2005).

Misuse of ABs is facilitated if beekeepers know where to purchase them and how to avoid the necessary legal route. AB acquisition was investigated and suggested some level of veterinary engagement, but beekeepers were primarily purchasing ABs from pharmacies (EU), the internet (US) or national bee inspectors (UK). The locations of purchase can often be indicative of illegal intent, especially when considering that 55% of US based websites selling antibiotics do not require a prescription according to Garcia et al. (2020). Undocumented trade and use of antimicrobial treatments could result in imprudent use of the product, leading to the development of superbugs, health issues within the hive and AB residues contaminating bee products (Bártíková et al., 2016).

Respondents in the US reported a significant use of ABs against EFB and less frequently against AFB. This finding is suggestive of general awareness regarding the long-lived spores of P. larvae which cannot be killed, but only temporarily controlled with antibiotics (Krongdang et al., 2017). Studies have in fact shown that while AB treatments can suppress symptoms of the disease, the spores remain in the environment surviving the treatment and eventually causing the hive to relapse (Krongdang et al., 2017).

The US, however, also indicated a higher use of ABs against Nosema for which no antibiotics are currently approved. In 2013 the FDA withdrew the application of approval for fumagillin (New Animal Drug Applications; Alfaprostol; Bicyclohexylammonium Fumagillin; N, 2013). Furthermore, a number of studies have reported a substantial increase in resistance and possible toxic effects of fumagillin suggested in both honeybees and humans (Rodriguez-Garcia et al., 2018; Burnham, 2019). A current lack of approved active ingredients for Nosema presents a significant demand for new medications that safely and effectively treat honeybee colonies against this pathogen (Burnham, 2019). Non-significant findings showed a general consensus regarding the function of antibiotics used for treating diseases as opposed to preventing them, suggesting appropriate use of ABs. Studies in fact show that prophylactic and metaphylactic use of antibiotics in production species have resulted in the development of resistant bacteria within the animals and their surrounding environments (Zhu et al., 2013; Larsson, 2014; Gonzalez Ronquillo & Angeles Hernandez, 2017). Similarly, all three geographic areas reported no statistical differences concerning the need for a prescription for antibiotics. However, the average response rate reached 60%, a lower rate compared to the small animal veterinary industry, where owners are more conscious of the need for a prescription when purchasing antibiotics. This usually occurs because pet owners are in direct contact with veterinarians that must provide prescriptions before dispensing medications (Redding & Cole, 2019). In beekeeping, veterinarians are often foregone either due to their lack of knowledge on honeybee pathologies or because veterinary consults may be deemed too expensive for beekeepers.

All three geographical areas reported having little to some knowledge of AB issues, with the UK self-reporting the lowest average knowledge. A general lack of knowledge was further supported by the results of a subsequent question investigating beekeeper understanding of AB function. The US indicated that ABs are mainly used to prevent diseases, a practice that is strongly discouraged by veterinary and health professionals worldwide, as prophylactic use often results in the development of resistance (Gonzalaz Ronquillo & Angeles Hernandez, 2017). The EU, instead, underreported AB use to target bacteria, indicating a lack of awareness regarding the correct function of antibiotics as medicines that target bacteria specifically. Misuse and overuse have been described as the major contributors to antibiotic resistance, suggesting the importance of beekeepers understanding AB function and correct use (Sifri et al., 2019). For this reason, it is necessary to ensure beekeepers have access to accurate information, ideally provided by reliable sources and trained experts.

The survey identified that only EU respondents sought veterinary advice on treatment, while the UK and US relied heavily on books and the internet. These findings show a stark contrast to other animal-related fields, where owners are more likely to consult a veterinarian prior to treatment (De Briyne et al., 2013). A persistent lack of beekeeper-veterinary rapport not only establishes a knowledge gap within the industry but further results in beekeepers seeking advice elsewhere, as seen in these results, often from other beekeepers that may be similarly deficient in antibiotic related knowledge (Williams, 2000). The UK, however, reported the involvement of national bee inspectors, who are trained to diagnose honeybee diseases, and are the only entity allowed to issue and administer ABs in the UK (Wilkins et al., 2007). Inspectors are also tasked with inspecting hives annually alongside randomly testing hive products and matrices for antibiotic residues, ensuring regular compliance of all beekeepers. The current findings would suggest that while AB use is generally dictated by legislation and mostly compliant, knowledge regarding AB issues is somewhat lacking. Awareness campaigns have already been adopted in multiple countries in an attempt to educate beekeepers as to the risks of antibiotic resistance, mostly through the National Bee Unit in the UK and extension services in the US, but efforts are still underway to increase their impact (Huttner et al., 2019).

When asked to report how often ABs fail to treat honeybees, the US reportedly witnessed this the most. Such a response is supported by the multiple studies that have indicated widespread resistance to the ABs commonly used in apiaries (Alippi et al., 1999; Krongdang et al., 2017). This finding also indicates beekeepers may be using ABs imprudently or adopting practices that increase the chance of resistance developing. Furthermore, the response rate from all three areas (40% EU, 76% US, 42% UK) would suggest that imprudent use of ABs is occurring more frequently than declared in previous questions. Beekeepers in the UK appeared consistently more aware and compliant throughout, further supported by an increased awareness of drug resistance infections, but respondents in the UK were also less aware of AB residues compared to those in the EU and US. This finding was perhaps less surprising since those in the UK also reported the lowest number of professional beekeepers (7%). A study by Jones et al. (2015), in fact, suggested that individuals that are economically affected by product contamination are generally more aware of residues, compared to hobbyists producing for themselves.

Most respondents agreed that contaminated products should not be consumed, with no statistical differences appearing between areas. This belief reflects the findings of a study assessing consumer perception regarding health and safety when consuming animal-derived products, suggesting that consumer demand for safer products highly influenced marketing and sale of such products (Kos Skubic et al., 2018). General consensus was similarly met regarding the belief that AB resistance would have a significant impact on various spheres of life. AB resistance has been shown to be an increasingly significant threat to medicine, veterinary medicine and the environment. Studies are reporting more frequent and severe cases of resistance in most medical fields, as well as high levels of residues in many bodies of water and soil samples (Martens & Demain, 2017; Jia et al., 2017).

Some limitations were considered alongside the need for further research. A more active distribution of the survey, with the involvement of additional beekeepers’ associations and social platforms would have prompted a larger population sample, providing more insight and more robust tests. However, the sample was large enough to produce valid results. The survey included both hobbyists and professional beekeepers, combining different practices since professionals often require more stringent biosecurity and resort more easily to ABs to maintain hive health throughout the year (Reybroek, 2012). The current study set out to assess the impact that legislation has on antibiotic use and awareness. It was not possible to discern significant differences caused by legislation, but the study was able to ascertain that ABs are apparently used by a small percentage of beekeepers in all three areas, regardless of the legislative context. Moreover, the analysis of the survey data identified a lack of in-depth AB awareness, suggesting that stronger campaigns are needed to increase widespread understanding of AB principles and related risks. The use of a globally distributed survey could continue to be employed as a risk-assessment tool, outlining shortcomings within the beekeeping community and allowing for a targeted approach in advancing sustainable beekeeping practices.