2.1. Complex amplitude of light wave and radiation intensity

The electromagnetic nature of the light waves was theoretically substantiated by British physicist Maxwell in his paper [15]. Ruling out the currents from his equation system, he obtained an equation that describes the propagation of electromagnetic disturbances:

$$
\overrightarrow{\Delta f} - \frac{\frac{1}{c^2} d^2 \overrightarrow{f}}{dt^2} = 0,\tag{1}
$$

where f ! is the electric E ! or magnetic H ! field vector tension, and с is light velocity.

Note that this equation exactly coincides with the equation of disturbance motion in elastic no compressive medium.

Further, let us target on plane monochrome waves that are a special case of a solution to Eq. (1). These are the waves wherein the electric and magnetic field vary according to the cosine law and vector f ! is a function of a single coordinate and time. Let us restrict ourselves to discussing the tension of the electric-filed vector. In a form independent from the origin selection for a plane monochrome wave, we have [16]:

$$\overrightarrow{E} = \text{Re}\{\overrightarrow{E}\_0 \mathbf{e}^{+i(\overrightarrow{k}\cdot\overrightarrow{r}-\omega t)}\},\tag{2}$$

where E ! 0 is some constant complex vector, k ! is a wave vector equaling ðω=cÞ n ! ¼ ð2π=λÞ n !, r ! is a radius vector of a point of space, ω is the wave frequency, λ is the wavelength, and n ! is a single vector coinciding with the direction of the light wave propagation.

Let us further accept that all the waves have the same direction of the electric field vectors, then, when the waves impose their amplitudes, they can be added as scalar values. Besides, further in Eq. (2), we shall omit symbol Re and operate exponents instead of cosines. It is possible because in the problems that we are discussing below the final result will differ by an insufficient factor. Instead of Eq. (2), we have:

$$E(\mathbf{x}, y, z, t) = A(\mathbf{x}, y, z) \exp\left(-i\omega t\right),\tag{3}$$

where expression Aðx, y, zÞ¼jAðx, y, zÞjexp½iθðx, y, zÞ� was named complex amplitude in optics, jAðx, y, zÞj is the module of the complex amplitude, and θðx, y, zÞ is the wave phase at the observation point.

Now let us introduce the notion of light intensity as a value proportionate to volumetric density of radiation energy averaged by the time interval substantially exceeding the wave oscillation period:

$$I(\mathbf{x}, y, z) = \lim\_{T \to \infty} \frac{1}{T} \int\_{-T/2}^{T/2} |E(\mathbf{x}, y, z, t)|^2 dt = |A(\mathbf{x}, y, z)|^2. \tag{4}$$

Thus, the radiation intensity at a point of space equals the squared complex amplitude module.

#### 2.2. Interference of two waves

Let us discuss the light intensity distribution in superposition of two monochrome waves. Suppose that two waves of the same length λ were emitted by one point source in various directions, then two plane waves 1 and 2 crossing at angle θ were shaped by the optical systems. Let us take some point in the area of beam superposition. For certainty, let the wave amplitudes be the same equaling A0, but their initial phases ϕ differ. In compliance with Eq. (4), we have:

$$I = A \times A^\* = \left[ A\_0 e^{i(\vec{k\_1}\vec{r} + \varphi\_1)} + A\_0 e^{i(\vec{k\_2}\vec{r} + \varphi\_2)} \right] \times \left[ A\_0 e^{-i(\vec{k\_1}\vec{r} + \varphi\_1)} + A\_0 e^{-i(\vec{k\_2}\vec{r} + \varphi\_2)} \right]$$

$$= 2I\_0 + 2I\_0 \cos\left[ (\vec{k\_1} - \vec{k\_2})\ \vec{r} + \varphi\_1 + \varphi\_2 \right],\tag{5}$$

where I0 ¼ A2 0. Eq. (5) describes periodic light intensity distribution in the neighborhood of point r !, which was called light interference by T. Jung. Elementary calculations can demonstrate [17, 18] that minimum distance Δ between neighboring intensity maximums or minimums called bandwidth or period of the interference fringes is determined by formula (Eq. (6)):

$$
\Delta = \frac{\lambda}{2\sin\frac{\theta}{2}}.\tag{6}
$$

It follows from Eq. (6) that if θ tends to zero, Δ tends to infinity, which corresponds to tuning of the interferometer to "endless" band. If angle θ between vectors k ! 1 and k ! 2 equals 180°, then Δ ¼ λ=2, which corresponds to the wave interference in colliding beams. For θ = 60° value, Δ ¼ λ.

Now let us discuss the contrast of the interference fringes γ introduced by Michelson and determined by formula γ ¼ ðImax−IminÞ=ðImax þ IminÞ, where Imin and I max are the minimum and the maximum intensity values, respectively. From Eq. (5), it follows that in the case of a point light source discussed here and constant wavelength λ, contrast γ ¼ 1. Experience shows that if the light source is not point and (or) it emits light in some wavelength interval, the fringes contrast is less than 1.

It is commonly believed that case γ ¼ 0 corresponds to completely incoherent light; if 0 < γ < 1, the light is partially coherent, and coherence is the ability of waves to interfere. Interference of partially coherent light can be studied in Ref. [19]. In the text below, we will suppose that the light waves discussed here are completely coherent, i.e., two waves of the same amplitude generate an interference pattern with the contrast equal to 1. We can suppose with practical precision that similar waves are generated by laser light sources.


**2. Types of agricultural biowastes**

Farm residues can be broadly divided into crop residues, and wastes from livestock and aquaculture depending on the activities carried out. Field crop residues are plant parts left over in the field without much attention unless otherwise is immediately followed by a succeeding crop. Crop residues can be put under

#### **Table 1.**

*Chemical composition of agri-industrial wastes [7].*

*Sustainable Biowaste Management in Cereal Systems: A Review DOI: http://dx.doi.org/10.5772/intechopen.97308*

agricultural and agri-industrial categories. Agricultural residues remaining after threshing and separation of the economic plant part(s) can be of (a) processed residues such as husks and hay and (b) field crop residues such as stalks and stubbles. Husk and hay are often left over in the crop field due to engagement of crop combined harvesters and axial flow threshers. Sometimes, the distance between crop field and farm house plays a decisive role in stacking of hay and husk in the crop field after threshing. That apart, farm mechanization in many developed countries has also shifted from animal driven to fossil fuel based farm power and thus excluding the need for gathering feedstock in the haystack. Furthermore, the risk of fire in haystack due to storage of dried crop residues can also not be eliminated completely. Hence, many farmers are not interested in transporting such bulky byproducts from crop field to farmhouse. In mono cropped areas, natural weathering and decomposition by soil organisms usually degrade the field crop residues but the residue management challenge is mostly under sequential cropping.

Agri-industrial residues in the other hand are derived from industries such as peels of potato, orange, and cassava; bagasse and molasses of sugarcane; oilcakes of groundnut, mustard, sunflower, sesame, soybean and coconut; and husks and bran of rice [7]. Huge quantities of organic wastes are produced by food and vegetable oil processing industries every year- but if left untreated and unutilized, may cause environmental pollution as well as human and animal health issues. A representative chemical analysis report of few agri biomass are depicted under **Table 1** for comparative studies.


**4. Conclusion**

In this work, we reviewed the deposition parameters and properties of titanium and titanium-aluminum-based quaternary coatings. It is found that the effect of the individual as well as multiple alloying elements are manifested in further modifying the properties of (Ti, Al) N coatings. Research and developments on simple binary and ternary coatings in previous studies are discussed. This was followed by the investigations on quaternary multicomponent coatings (TiAlZrN/TiAlN/TiAl and TiAlCN/TiAlN/TiAl); the behaviors in these coatings in fretting wear are compared. The main conclusions are the following. The local card solicitation obtained for the two layers of quaternary studied shows the delimitation of both sliding rates. It is shown that the gross slip regime region (GSR) of the coated AISI4140 steel is extended by the presence of the TiAlZrN layer in comparison with the TiAlZrN layer. These results are being very useful in the tribology. Indeed, the GSR is always associated to wear, but the partial slip regime (PSR) is accompanied to a crack that can be disastrous and leads to the failure. To reduce the instantaneous friction coefficient and stabilized friction coefficient, it is necessary to choose the coating-based zirconium coating instead of the coating-based carbon. In general, the stability of the coefficient of friction observed under the fretting conditions tested for a PVD coating was linked to the presence of a third multilayer body: a first layer consisting of particles mainly of submicron size; a second, discontinuous lamellar layer; and a third layer consisting of particles having a microstructure with ultrafine grains (refinement). In steady state, the third body formed easily remains trapped in contact. The third body, less than 50 μm thick, protects the surface (reduced wear) and is stable.

However, the gap between these two coatings is governed by the amplitude of the loading parameters. The thin coatings formed by physical vapor deposition may provide an initial friction reduction but it is not sufficiently durable for this application. However, the beneficial effect of the PVD coatings on fretting wear diminishes with increasing normal force and decreasing fretting stroke. In this chapter, the worn volume of the two quaternary layers is very influenced by loading conditions. Therefore, special attention should be given to better distinguish the effect of zirconium. Adding Zr improves the wear resistance of Al-Ti-N coating. Zr stabilizes Ti-Al-N lattice and also forms a very thin stable oxide layer similar to Al2O3. These two effects together enhance the wear resistance of the Ti-Al-Zr-N coatings. The

stability of the energy approach is used to predict the wear kinetics in a volume of tribo-systems: Wv = α × Ed Σ, where, α is the energetic coefficient, Wv is the worn volume, and Ed is the dissipated cumulated energy. The multilayered TiAlZrN/ TiAlN/TiAl coatings improve the resistance to the fretting wear of AISI4140 steel by twice as much as the multilayered TiAlCN/TiAlN/TiAl coatings.

In the light of various experimental investigations, the study of the wear mechanisms of the different films was carried out. It follows that the advantages of a multilayer coating over a single-layer coating are mainly presented in three points:


**Comparing Hospital and Primary Care Physicians' Attitudes and Knowledge Regarding Antibiotic Prescribing: A Survey within the Centre Region of Portugal**

**António Teixeira Rodrigues 1,2, João C. F. Nunes 3 , Marta Estrela 1 , Adolfo Figueiras 4,5,6 , Fátima Roque 7,8,\* and Maria Teresa Herdeiro 1**

**Abstract:** Background: Antibiotic resistance is a worldwide public health problem, leading to longer hospital stays, raising medical costs and mortality levels. As physicians' attitudes are key factors to antibiotic prescribing, this study sought to explore their differences between primary care and hospital settings. Methods: A survey was conducted between September 2011 and February 2012 in the center region of Portugal in the form of a questionnaire to compare hospital (*n* = 154) and primary care (*n* = 421) physicians' attitudes and knowledge regarding antibiotic prescribing. Results: More than 70% of the attitudes were statistically different (*p* < 0.05) between hospital physicians (HPs) and primary care physicians (PCPs). When compared to PCPs, HPs showed higher agreement with antibiotic resistances being a public health problem and ascribed more importance to microbiological tests and to the influence of prescription on the development of resistances. On the other hand, PCPs tended to agree more regarding the negative impact of self-medication with antibiotics dispensed without medical prescription and the need for rapid diagnostic tests. Seven out of nine sources of knowledge's usefulness were statistically different between both settings, with HPs considering most of the knowledge sources to be more useful than PCPs. Conclusions: Besides the efforts made to improve both antibiotic prescribing and use, there are differences in the opinions between physicians working in different settings that might impact the quality of antibiotic prescribing. In the future, these differences must be considered to develop more appropriate interventions.

**Keywords:** hospital care; primary care; physicians; antibiotic; prescription; Portugal

### **1. Introduction**

Antibiotic resistance is a worldwide public health problem, leading to longer hospital stays and raising medical costs and mortality levels [1–5]. Previous studies highlighted the role of the over-prescription and mis-prescription of antibiotics on the development of resistances [6–11]. Hence, promoting interventions to improve the antibiotic prescribing process is a key element to improving antibiotic use and diminishing resistances.

To improve the effectiveness of antimicrobial stewardship interventions, their design should be multifaceted, multidisciplinary and based on the characteristics of each specific

**Citation:** Rodrigues, A.T.; Nunes, J.C.F.; Estrela, M.; Figueiras, A.; Roque, F.; Herdeiro, M.T. Comparing Hospital and Primary Care Physicians' Attitudes and Knowledge Regarding Antibiotic Prescribing: A Survey within the Centre Region of Portugal. *Antibiotics* **2021**, *10*, 629. https://doi.org/10.3390/ antibiotics10060629

Academic Editor: Seok-Hoon Jeong

Received: 13 April 2021 Accepted: 23 May 2021 Published: 25 May 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

setting [12–14]. However, prescribing is a complex process, usually affected by economic, demographic, clinical, cultural and social factors beyond evidence-based recommendations [6].

Attitudes are the key factors in the antibiotic prescribing process [13,15,16]. However, an in-depth understanding of how attitudes affect physicians' clinical practice in different settings is needed. To our knowledge, there are no studies assessing the differences between attitudes and knowledge of hospital physicians (HPs) and primary care physicians (PCPs). Therefore, the aim of this study was to compare both the attitudes and knowledge between PCPs and HPs with regards to antibiotic prescribing.

#### **2. Materials and Methods**

#### *2.1. Study Design, Population and Ethics Statement*

A survey was conducted in Portugal's Centre Regional Health Administration (ARS-Centro) (Population in 2011: ~1,737,059 people), from September 2011 to February 2012. Determinants of prescribing were assessed in all PCPs working in the National Health Service facilities of the ARS-Centro and hospital care physicians working in internal medicine departments within the hospitals of the ARS-Centro.

This study was approved by Portugal's Centre Regional Health Administration (Permit No. 015650/2011), by the hospital's administration and by the Portuguese Data Protection Authority (Comissão Nacional de Proteção de Dados/CNPD) (Permit No. 2886/2013). The personally addressed, reply-paid self-administered questionnaires were sent by post mail to PCPs up to four times to nonrespondents. In the case of HPs, the questionnaires were hand-delivered to the director of each hospital/medical service, who distributed them among the HPs. The answers were then collected by the administrative services of the department. The respondents did not receive any incentives. Nine hundred and fourteen questionnaires were delivered to PCPs and two hundred and twenty-seven questionnaires to HPs. All the data concerning PCPs' knowledge and attitudes has been previously published [15].

#### *2.2. Data Collection*

All physicians were asked to fill a previously validated (published elsewhere [16,17]), two-page long questionnaire, divided into 5 sections:

The measurement of the agreement with the questions included in Sections 2 and 3 of the questionnaire was performed through a horizontal, continuous visual analog scale, 8 cm long and unnumbered [16]. Answers were converted into a range from zero (total disagreement) to ten (total agreement). Physicians confidentiality was guaranteed.

#### *2.3. Statistical Analysis*

As the variables did not follow a normal distribution, nonparametric tests were conducted. Differences in the results between HPs and PCPs were evaluated using the Mann–Whitney *U* test. Differences were established as statistically significant at *p* < 0.05. The statistical analysis was performed using SPSS 25 (SPSS Inc., Armonk, NY, USA) and MS Excel (Microsoft Corporation, Redmond, WA, USA) software.

#### *2.4. Sensitivity Analysis* In order to assess whether the differences observed were influenced by the fact that some physicians reported to work on both settings, a sensitivity analysis was conducted,

*2.4. Sensitivity Analysis*

*2.3. Statistical Analysis*

In order to assess whether the differences observed were influenced by the fact that some physicians reported to work on both settings, a sensitivity analysis was conducted, in which these physicians were excluded. in which these physicians were excluded. **3. Results**

As the variables did not follow a normal distribution, nonparametric tests were conducted. Differences in the results between HPs and PCPs were evaluated using the Mann– Whitney *U* test. Differences were established as statistically significant at *p* < 0.05. The statistical analysis was performed using SPSS 25 (SPSS Inc., Armonk, NY, USA) and MS

*Antibiotics* **2021**, *10*, x FOR PEER REVIEW 3 of 11

Excel (Microsoft Corporation, Redmond, WA, USA) software.

#### **3. Results** The overall response rate was 47.8%: of the PCPs; 421 answers were obtained, which

The overall response rate was 47.8%: of the PCPs; 421 answers were obtained, which corresponded to an overall response rate of 46.1%; 124 of the HPs invited accepted to participate in the study, corresponding to an overall response rate of 54.6%. corresponded to an overall response rate of 46.1%; 124 of the HPs invited accepted to participate in the study, corresponding to an overall response rate of 54.6%. The process of distributing and collecting the questionnaires is summed up in the

The process of distributing and collecting the questionnaires is summed up in the Figure 1 below. Figure 1 below.

**Figure 1.** Questionnaire distribution and collection flowchart. **Figure 1.** Questionnaire distribution and collection flowchart.

*3.1. Comparison of Sociodemographic and Professional Characteristics*

*3.1. Comparison of Sociodemographic and Professional Characteristics*  Table 1 presents the comparisons between the sociodemographic characteristics of Table 1 presents the comparisons between the sociodemographic characteristics of PCPs and HPs.

#### PCPs and HPs. **Table 1.** Sociodemographic and professional characteristics of both primary care and HPs. *3.2. Comparison of Knowledge and Attitudes towards Antibiotic Prescribing, Antibiotic Use and Antimicrobial Resistance*

 **PCPs HPs**  Table 2 describes and compares the results obtained for the 17 statements concerning antibiotic prescribing and resistances in both PCPs and HPs.

**Age (years)** Median 55 (421/100%) 40 (124; 99.2%) **Gender** Statistically significant results were obtained for the attitudes such as ignorance, responsibility of others, fear, complacency and indifference statements. Regarding ignorance, hospital physicians showed a higher agreement with resistance being a public health problem (S1), the importance of microbiological tests (S2) and the influence of prescriptions on the development of resistances (S4) compared to PCPs.

**Table 1.** Sociodemographic and professional characteristics of both primary care and HPs.

About the responsibility of others, HPs appear to be less convinced that the development of new antibiotics will solve the resistance problem (S5). On the other hand, PCPs tend to agree more regarding the negative impact of self-medication with antibiotics and dispense without medical prescription (S12 and S13). Furthermore, PCPs expressed a higher agreement about the need of rapid diagnostic tests (S3).

PCPs agreed more with the prescription of antibiotics in situations of fear and uncertainty (S7 and S8), as well as about having a complacent attitude with their patients (S10).

#### *3.3. Comparison of the Usefulness of Different Sources of Knowledge*

Table 3 describes and compares the results regarding the usefulness of different sources of knowledge between primary care and HPs.

The differences found in the usefulness of sources of knowledge were all related to HPs considering some of the sources evaluated more helpful. Differences were found for clinical practice guidelines, documentation from the industry and from medical information officers, continuous educations, contribution of specialists, peers and the internet.

**Table 2.** Differences in the attitudes and knowledge regarding antibiotic prescribing between PCPs and HPs (10—completely agree; 0—completely disagree).

**Table 3.** Differences in the usefulness of sources of knowledge between primary care and HPs (10—completely agree; 0—completely disagree).

#### *3.4. Sensitivity Analysis*

Overall, after the sensitivity analysis, the differences between PCPs and HPs, have remained constant in almost all dimensions. However, the attitudes of fear (S7) and responsibility of others—other professionals (S13) were no longer significant. Furthermore, despite that the distribution remained the same as the one reported in Table 2, the differences between the importance attributed to Continuing Education Courses (S6) were no longer significant.

#### **4. Discussion**

This study shows that, besides an overall increasing of both apprehension and knowledge regarding health professionals and patients, there are still differences in the knowledge and attitudes that may be important to tackle in future healthcare interventions [18,19]. Furthermore, and considering that antibiotics can only be prescribed by physicians, these results provide a picture on the discrepancies between HPs and PCPs in terms of attitudes and knowledge concerning antibiotic resistances.

Regarding the attitudes underlying antibiotic prescribing, statistically significant differences were found for the responsibility of others, fear, indifference, complacency and ignorance in 12 of the 17 statements evaluated. These constitute somewhat unsettling results, as it reveals how different the attitudes concerning resistance between both settings can be.

Most HPs and PCPs agreed that antibiotic resistance is an important public health problem in their settings, reflecting the knowledge regarding antibiotic resistance is a distressing worldwide public health problem, increasing medical costs and mortality levels [3–5,20,21]. However, significant differences were found between HPs and PCPs, where the HPs showed higher agreement with the statement. This fact might be related with the challenges that HPs are facing to hamper and control the spread of resistant infections and their treatment in their setting. HPs also showed higher knowledge when considering the impact of a prescription to a patient as a factor underlying the possible appearance of resistance. Prior evidence revealed antibiotic prescriptions and use as selective pressure driving at this resistance, both on an individual [22] and community level [23].

The development of new antibiotics is also a point of discordance between PCPs and HPs: the first are more convinced that new antibiotics will be developed, and the literature shows promising lines of research [24]. However, the evidence shows the importance of conserving the molecules already available in practice, namely by using them wisely.

Significantly different answers were also obtained regarding the usefulness of the microbiology results in deciding which treatment to provide and the availability of the

diagnostic techniques. The results of blood cultures help to reduce antibiotic use and narrow antibiotic therapy, thus reducing the costs [25], and there are several emerging potential technologies that can address the clinical needs [26]. Nevertheless, the differences found might be related to the availability of diagnostic techniques in time in the hospital setting, contrarywise to what is found in primary care settings, in which widespread testing is not feasible. Yet, in some specific diseases—namely, for pharyngitis—rapid antigen testing is recommended before an antibiotic prescription [27–31].

Differences were also found regarding the responsibility of patients or pharmacies, where PCPs agreed more that patients may manage to obtain antibiotics even without a prescription and/or self-medicate. This difference in physicians' perceptions might be related to the proximity between primary care and community pharmacy practices. Nevertheless, the evidence is published about the dispense without a prescription [32,33] and self-medication with antibiotics [34], which leads to antibiotic misuse and resistances.

Fear about future bacterial resistances was also an attitude where physicians showed differences. PCPs agreed more about prescribing broad-spectrum antibiotics, in the case of diagnostic uncertainty or the impossibility of following-up patients. This might be explained with the unavailability of diagnostic tools to aid physicians' diagnosis in primary care settings and is concordant with the previous research [6,35–37].

The statistically significant opinions in which physicians showed the least agreement were related to insistence from the patient, patient trust and time constraints. Again, differences were found, and PCPs seem to be more complacent with patients than the HPs. There is data indicating that both physicians consider patient satisfaction is crucial, so it is vital to manage patients' expectations [9,38], namely with emphasis on precise clarifications. As a patient's satisfaction is related to their belief of their understanding of their disease, the data shows the success of longer, patient-centered consultations with low antibiotic prescriptions [6,8,9,13,39,40]. Changing primary healthcare setting is hard, but patient empowerment and reinforcement during doctor–patient communication with a realist awareness of the patient's expectations was reveal to be essential in reducing the antibiotic prescription [41,42].

HPs tended to show higher agreement about the usefulness of the sources of knowledge. With exception to the courses promoted and organized by the pharmaceutical industry and previous clinical practices, all the other sources of knowledge evaluated were considered more useful by HPs. The reasons behind these differences are complex to understand, but the need to be continuously updated in a hospital care context might be associated with the results found. Furthermore, as the HPs tended to be younger, they might feel the need to resort to other sources of knowledge to compensate for a lower clinical practice experience when compared to PCPs, who tend to be older. Perhaps younger doctors rely more on sources of information based on scientific evidence, while older doctors rely on their clinical experience.

Considering the fact that the vast majority of antibiotics are prescribed in primary care [43], the identification of the differences in the attitudes and the underlying behaviors in antibiotic prescribing between settings allows us to tailor antibiotic stewardship interventions. As inadequate antibiotic prescriptions are an important factor for antibiotic resistances development [18,19], and high rates of inadequate antimicrobial prescribing are noted in the context of primary care [44], identifying the dimensions in which PCPs are less aware is an essential strategy toward improving these issues. Furthermore, parallel to the results in this study, in which PCPs tend to attribute more responsibility to others than HPs, and less important than the issue of antibiotic resistances, some studies have shown that PCPs do not only give less importance to the issue of antibiotic resistances but also tend to not consider themselves particularly accountable about their roles in this issue [20,21,44]. Hence, raising awareness among PCPs to tackle antimicrobial resistances should be a priority.

This study is accompanied by some limitations. Despite the statistically significant differences in attitudes, we cannot assure it triggers different antibiotic prescribing practices

between settings. Considering the geographical limitations, the low response rate and specific characteristics regarding physicians' clinical practice and the Portuguese Health System, the extrapolation of the results to other countries might not be adequate, as it can compromise its external validity. Nevertheless, the internal validity has been assured, as the questionnaire has been previously validated [16,45]. The response rates obtained both with primary care and HPs are low when compared to similar studies [46–48]. However, low response rates among physicians is a recognized problem in survey research [49,50]. The fact that the questionnaires were sent by post mail to PCPs and hand-delivered to the director of each hospital/service, along with the differences in the geographical dispersion of physicians within the territory, might explain the slight discrepancy between the response rates. Still, the difference in only 8% between response rates constitutes a positive outcome in this study, as it results in a less-biased appraisal between both settings. Furthermore, at the time in which this survey was conducted, there were 4.5 physicians/1000 inhabitants, considering both the public and private sectors [51]. Considering the estimated population of the center region, we estimate that this survey is highly representative of the public sector physician population, as it included almost a third of the physicians of this region. Even though this study was conducted in 2011 to 2012, which can be considered a limitation, the data from this study remains relevant, as the attitudes are stable variables over time [20,21], and it still brings an important contribution to the knowledge on this topic.

#### **5. Conclusions**

To conclude, the results of the study revealed that there are differences in opinions between physicians working in hospital and primary care that might impact the quality of antibiotic prescribing. Therefore, interventions to improve the antibiotic prescription quality should be tailored to each setting, especially considering the more evident differences between primary care and HP attitudes (particularly, dimensions of fear, ignorance and responsibility to others) for a more effective tackling of this global concern.

**Author Contributions:** Conceptualization, A.F., F.R. and M.T.H.; data curation, A.T.R., F.R. and M.T.H.; formal analysis, A.T.R., J.C.F.N., M.E., A.F., F.R. and M.T.H.; funding acquisition, F.R. and M.T.H.; investigation, A.T.R., A.F., F.R. and M.T.H.; methodology, A.T.R., J.C.F.N., M.E., A.F., F.R. and M.T.H.; project administration, M.T.H.; writing—original draft, A.T.R. and writing—review and editing, J.C.F.N., M.E., A.F., F.R. and M.T.H. All authors have read and agreed to the published version of the manuscript.

**Funding:** This work was supported by the Foundation for Science & Technology (Fundação para a Ciência e Tecnologia—FCT), Institute of Biomedicine -iBiMED (UIDP/04501/2020) grant (UIDB/04501 /2020) and by grant PTDC/SAU-ESA/105530/2008, from the Portuguese Ministry of Science & Education, co-financed by FEDER through the COMPETE Program, and by the research project PTDC/SAU-SER/31678/2017, supported by the operational program on competitiveness and internationalization (POCI) in its FEDER/FNR component, POCI-01-0145-FEDER-031678, and by the Foundation for Science and Technology in its state budget component (OE).

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki and approved by approved by Portugal's Centre Regional Health Administration (Permit No. 015650/2011), by the hospital's administration and by the Portuguese Data Protection Authority (Comissão Nacional de Proteção de Dados/CNPD) (Permit No. 2886/2013).

**Informed Consent Statement:** The participation of the questionnaire was a volunteer and only the participants that agree to participate fulfill the questionnaire.

**Acknowledgments:** We thank Tânia Magalhães Silva (iBiMED/UA) for her collaboration on the revision of the manuscript.

**Conflicts of Interest:** The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses or interpretation of the data; in the writing of the manuscript or in the decision to publish the results.

### **References**

## *Article* **Knowledge and Attitudes about Antibiotics and Antibiotic Resistance of 2404 UK Healthcare Workers**

**Diane Ashiru-Oredope 1,\* , Ella Casale 1 , Eleanor Harvey 1 , Eno Umoh 1 , Sagar Vasandani 1 , Jacqui Reilly 2,3 and Susan Hopkins 1**

**Abstract:** Background: Using the COM-B model as a framework, an EU-wide survey aimed to ascertain multidisciplinary healthcare workers' (HCWs') knowledge, attitudes and behaviours towards antibiotics, antibiotic use and antibiotic resistance. The UK findings are presented here. Methods: A 43-item questionnaire was developed through a two-round modified Delphi consensus process. The UK target quota was 1315 respondents. Results: In total, 2404 participants responded. The highest proportion were nursing and midwifery professionals (42%), pharmacists (23%) and medical doctors (18%). HCWs correctly answered that antibiotics are not effective against viruses (97%), they have associated side effects (97%), unnecessary use makes antibiotics ineffective (97%) and healthy people can carry antibiotic-resistant bacteria (90%). However, fewer than 80% correctly answered that using antibiotics increases a patient's risk of antimicrobial resistant infection or that resistant bacteria can spread from person to person. Whilst the majority of HCWs (81%) agreed there is a connection between their antibiotic prescribing behaviour and the spread of antibiotic-resistant bacteria, only 64% felt that they have a key role in controlling antibiotic resistance. The top three barriers to providing advice or resources were lack of resources (19%), insufficient time (11%) and the patient being uninterested in the information (7%). Approximately 35% of UK respondents who were prescribers prescribed an antibiotic at least once in the previous week to responding to the survey due to a fear of patient deterioration or complications. Conclusion: These findings highlight that a multifaceted approach to tackling the barriers to prudent antibiotic use in the UK is required and provides evidence for guiding targeted policy, intervention development and future research. Education and training should focus on patient communication, information on spreading resistant bacteria and increased risk for individuals.

**Keywords:** anti-infective; antimicrobial; antimicrobial resistance; behaviour change; healthcare workers; antimicrobial stewardship

### **1. Introduction**

In England, antimicrobial resistant infections increased between 2016 and 2019, peaking at an estimated 65,192 infections in 2019 [1]. Nationally and internationally, several policy papers have emphasised the need to address this globally recognised, complex threat to human health [2–5]. The UK's five-year National Action Plan (NAP) to tackle antimicrobial resistance (AMR) emphasises the importance of reducing our need for, and exposure to, antimicrobials, and optimising the use of these life-saving drugs in humans and animals. Healthcare workers' (HCWs') practices impact infections and antimicrobial use; therefore, they are vital in our efforts to tackle AMR. Moreover, HCWs play an instrumental role in implementing antimicrobial stewardship interventions, highlighting the necessity of understanding their knowledge, attitudes and behaviour towards antibiotics, antibiotic use and AMR.

**Citation:** Ashiru-Oredope, D.; Casale, E.; Harvey, E.; Umoh, E.; Vasandani, S.; Reilly, J.; Hopkins, S. Knowledge and Attitudes about Antibiotics and Antibiotic Resistance of 2404 UK Healthcare Workers. *Antibiotics* **2022**, *11*, 1133. https://doi.org/10.3390/ antibiotics11081133

Academic Editor: Marc Maresca

Received: 30 June 2022 Accepted: 5 August 2022 Published: 21 August 2022

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To support HCWs in tackling AMR, Public Health England (PHE) published a resources toolkit aimed at healthcare workers in 2014, which outlines key actions HCWs can take to help combat AMR [6]. Studies and public health campaigns that investigate and target the general public's knowledge and understanding of antibiotics and antibiotic resistance have been conducted [7,8]. The literature reports good basic knowledge with areas for improvement, such as targeting the misunderstanding that these drugs can be used to treat viral infections [9,10]. Evidence also exists for a subset of medical prescribers and nurses. Earlier studies have reported good knowledge of antibiotics among nurse practitioners and their intention to prescribe antibiotics appropriately [11,12]. Factors impacting nurse and physician prescribing have included patient pressure, fear, complacency and time [12,13]. Although there is some evidence for medical prescribers and nurses, a gap remains in the literature regarding multidisciplinary HCWs' knowledge, attitudes and behaviours towards this topic [11–15].

The European Centre for Disease Prevention and Control (ECDC) funded the first multiprofessional study across 30 European Union (EU) and European Economic Area (EEA) countries to assess HCWs' baseline knowledge, attitudes and behaviours surrounding antibiotics in 2019. This paper presents the results for the United Kingdom and aims to:

#### **2. Materials and Methods**

This study was part of a wider 2019 ECDC-funded survey across 30 EU/EEA countries. The full methodology is described elsewhere [16,17]. Using the COM-B model of behaviour change as a framework, this study sought to understand the capabilities (C), opportunities (O) and motivations (M) which enable prudent behaviour (B) about antibiotic use amongst healthcare workers in the UK [18].

The COM-B model was selected to underpin the questionnaire and analysis because it is a comprehensive synthesis and integration of at least 19 models of behaviour change [19]. The COM-B model proposes that behaviour is an interaction involving three essential components: the 'capability' (C) to perform the behaviour and the 'opportunity' (O) and 'motivation' (M) to carry out the behaviour. Studies of the model have shown that to affect behaviour change, any introduced interventions must influence as least one of these three components, so as to reshape behaviour and minimise setbacks [18].

The final questionnaire is available in the Supplementary Materials. Perceived and actual capability were measured to assess HCWs' knowledge. Perceived capability was assessed via self-reported understanding of antibiotic use and antibiotic resistance; participants were asked 3 questions about their own understanding. Actual capability was assessed via a 7-question knowledge test, with additional questions to assess one health and hand hygiene topics. Participants were asked 3 opportunity statements to assess whether they have the opportunity to contribute to tackling AMR; these focused on access to guidelines and materials and whether they were able to provide advice to patients. Motivation statements were utilised to assess attitudes towards antibiotics and their use. Behaviour investigated included the frequency of prescribing and whether HCWs gave out resources and advice.

A Project Advisory Group (PAG) consisting of 87 nominated individuals across 51 organisations and countries within the EU and EEA was established in 2018, of these 2 were

from the UK. Following a systematic review of the literature, the PAG participated in a two-round Delphi consensus process to develop the questionnaire tool. The final 43-item questionnaire was developed following a pilot of the survey across the EU/EEA, translation into 25 European languages and validation.

PAG members disseminated the validated online survey to HCWs in each of the 30 included countries. Multiple dissemination routes were used in the UK including email cascade via national AMR groups with representation from multidisciplinary professional groups asking them to cascade wider and social media, using the hashtag #ECDCAntibioticSurvey on Twitter. The information provided to survey participants is available in the Supplementary Materials. The questionnaire was live for 6 weeks, from 28 January to 4 March 2019. Participation was voluntary. Data were collected anonymously, with the option to submit contact details. Public Health England was responsible for housing all data securely and as per the General Data Protection Regulation 2016/679.

The statements used a five-point Likert score; for the purposes of this report, agreed and strongly agreed were merged in the text and reported as agreed.

The minimum survey sample size was obtained via quota sampling with the aim of generating a representative sample from different healthcare worker groups and countries and capturing different demographics, specialties, levels of experience and sectors of healthcare [16]. The sample size for the UK was calculated by determining 0.2% of practicing physicians (365/182,534), dentists (70/34,867) and pharmacists (113/56,542) and 0.1% of nursing professionals (548/548,291) available through EU/EEA healthcare personnel statistics of healthcare workers [17,20].

Data were analysed using Microsoft® Excel (2010) and STATA release 15. Descriptive statistical analysis was undertaken to analyse HCW capability, opportunity, motivation and behaviour.

The results of the UK study were shared with thirty-four attendees across the UK devolved administrations in June 2020 to inform recommendations.

Ethical statement: The data for this study were extracted from and comply with the ethical statement for the research undertaken by Ashiru-Oredope et al. [16]. Informed consent was provided prior to participation. The original study was part of an evaluation of the EU EAAD communications campaign which commenced in 2008 and included significant input in development and distribution from the PAG. The PAG officially represented all participating countries and European professional groups and organisations.

#### **3. Results**

#### *3.1. Demographics*

In the EU/EEA multicountry study, 18,365 HCWs responded to the online survey. Of these, 2404 participants were from the UK, equating to 13% of the EU/EEA total and the largest proportion among all 30 countries involved. The highest number of responses was collected from England (51%), followed by Scotland (40%), Wales (7%) and Northern Ireland (2%) (Supplementary Table S1). The highest number of participants stratified by English region were from the North West (23%), London (15%) and the South West (12%) (Supplementary Figure S1).

The UK exceeded its quota sample size by 979 responses, achieving 174% of the desired target (Supplementary Table S2). In England, Scotland and Wales, nursing professionals (nurses, nursing assistants and midwives) had the highest response rate (40%), followed by pharmacists (22%) and medical doctors (18%) (Supplementary Table S3). In Northern Ireland, pharmacists constituted the largest respondent group, followed by medical professionals and scientists. Healthcare students were not included in this sample.

Similarly to the EU/EEA survey results, most UK participants were female (77%), 21% were male and 1% preferred not to state their sex (Supplementary Table S4). UK respondents were mostly aged between 36 and 55 years (59%), 23% were under 36 years and 17% over 55 years. Respondents predominantly practised in hospitals (58%) or the community (31%).

In total, 24% of UK respondents used Facebook and 23% used Twitter for professional purposes. (Supplementary Table S5). Almost half of UK respondents (44%) did not use any social media for professional purposes.

#### *3.2. Perceived Capability*

The majority (96%) of UK respondents agreed or strongly agreed that they 'know what antibiotic resistance is' (Figure 1). Over three-quarters (78%) agreed or strongly agreed that they had sufficient knowledge on using antibiotics in their practice, and 80% agreed or strongly agreed that they know what information to provide to their patients on the prudent use of antibiotics and antibiotic resistance.

#### *3.3. Actual Capability Assessed by Seven Knowledge Test Questions*

The highest proportion of correct answers in the UK were given to the true or false questions: 'Antibiotics are effective against cold and flu' (answer = false) (98% false and 2% true); 'Taking antibiotics has associated side effects or risks such as diarrhoea, colitis, allergies' (answer = true) (97% true and 3% false); and 'Unnecessary use of antibiotics make them become ineffective' (answer = true) (97% true and 3% false) (Figure 2). Over 90% of HCWs knew that healthy people can carry antibiotic-resistant bacteria.

The question that was answered incorrectly by the most respondents was 'Antibiotic resistant bacteria can spread from person to person' (answer = true) (22% of respondents incorrectly answered false), which was higher than the percentage of incorrect answers from the EU/EEA respondents (13%) for that same question. The second statement with the most incorrect answers in the UK was 'Every person treated with antibiotics is at an increased risk of antibiotic resistant infection' (answer = true) (20% incorrectly answered false); this question had a higher rate of incorrect answers from the EU/EEA respondents (25%).

**Figure 2.** Percentage of UK (*n* = 2403) and EU/EEA respondents (*n* = 18,348) correctly answering the seven knowledge test questions.

In total, 59.4% of UK participants were able to answer all seven knowledge questions correctly. The EU/EEA average was 58%.

The answers to the knowledge test questions varied across professional groups. Medical doctors demonstrated the best knowledge of AMR (80% answered all questions correctly), followed by pharmacists (74%), dentists (68%) and scientists (62%) (Supplementary Figure S2). Only medical doctors had all the representatives scoring a minimum of five out of seven correct answers. Questions 5 and 6 were answered most correctly by medical doctors (86% and 96%, respectively (Supplementary Figure S3).

The percentage of respondents answering all seven questions correctly varied across the devolved administrations (54–80%). Northern Ireland had the highest proportion of respondents answering all seven questions correctly (80%, *n* = 41) (Supplementary Table S6). Across the EU/EEA, no country had 100% of respondents achieve 7/7 in the knowledge score.

Less than a quarter (23%) of UK participants correctly answered that the use of antibiotics to stimulate growth in farm animals is illegal in the EU (Supplementary Table S7). Almost half of respondents said they could list the WHO's five moments of hand hygiene (Supplementary Table S8).

#### *3.4. Opportunities*

Four out of five (80%) UK respondents stated having easy access to guidelines, compared to 75% of EU/EEA participants (Table 1). Only 62% of practitioners in the UK felt they have good opportunities to provide advice on prudent antibiotic use to individuals, compared to 72% of EU/EEA participants.

**Table 1.** Percentage of respondents who agreed or strongly agreed with the opportunity statements.

#### *3.5. Motivation/Attitude towards Antibiotic Resistance*

The majority (81%) of respondents who were prescribers agreed there was a connection between their prescribing and the emergence and spread of antibiotic-resistant bacteria, yet only 64% felt they have a key role in controlling antibiotic resistance (Supplementary Figure S4).

Across the devolved administrations, the percentage of survey participants agreeing with the motivation statements varied, ranging from 79% in Wales to 88% in Northern Ireland (Supplementary Figure S5).

#### *3.6. Behaviour (Giving out Resources or Advice) and Barriers*

In total, 59% of UK respondents had prescribed, administered or dispensed antibiotics at least once in the previous week (Supplementary Table S9), while almost 14% of the UK participants had not prescribed, administered or dispensed any antibiotics.

Of the prescribers, 21% had given out resources (e.g., leaflets or pamphlets) and 61% had given out advice on prudent antibiotic use at least once in the previous week to participating in the survey (Supplementary Figure S6).

The most common reasons respondents (*n* = 1671) gave for not providing resources or advice as frequently as they prescribed, administered or dispensed antibiotics were lack of resources (19%), insufficient time (11%) and the patient being uninterested in the information (7%) (Supplementary Table S10). Only 8% of HCWs stated they were able to give out advice or resources as needed.

#### *3.7. Awareness of National Initiatives and Campaigns, and Perceived Effectiveness*

Almost two-thirds (63%) of survey participants agreed that there has been good promotion of prudent antibiotic use and antibiotic resistance in the UK (Supplementary Figure S7). The results varied among HCWs across the devolved administrations (Supplementary Figure S8), with the most respondents agreeing from Northern Ireland (76%) and the least from Wales (54%).

Fifty-eight percent of UK respondents were aware of the National Action Plan (Figure 3). Less than half of respondents were aware of either EAAD (46% aware) or WAAW (45%), and approximately 30% felt that national campaigns had been effective. Respondents in the UK were mostly undecided (55%) on the campaign's effectiveness. Comparative data for the EU/EEA is available in Supplementary Figure S9. Focusing in on the UK constituent countries, participants from England agreed the most that national campaigns are effective (32%), whereas participants from Northern Ireland disagreed the most (24%) (Supplementary Figure S10).

Across the UK as a whole, the most commonly known resources were the National Institute for Health and Care Excellence (NICE) guidelines (49%), Treat Antibiotics Responsibly, Guidance, Education and Tools (TARGET) (31%) and Antibiotic Guardian (30%) (Figure 4). The most commonly used resources were the NICE guidelines (34%), resources other than those listed (32%) and Antibiotic Guardian (AG) (24%). Across the devolved nations results varied; however, NICE guidelines were the most commonly known and used resource across the four countries (Supplementary Figure S11).

In total, 49% percent of respondents stated they were Antibiotic Guardians; however, only 21% could recall their pledge (Supplementary Figure S12). Results varied across the four nations; England had the highest percentage of Guardians (56%) and Scotland the lowest (31%) (Supplementary Figure S12). Over three-quarters (76%) of UK HCW respondents

had seen or heard the KAW advert on television (TV) or radio (Supplementary Figure S13).

**Figure 3.** Awareness of campaigns in the UK; NAP (*n* = 2060), EAAD (*n* = 2070) and WAAW (*n* = 2054).

**Figure 4.** Awareness of campaigns, projects and platforms related to antibiotic use and AMR in the UK.

Less than a third (29%) of UK respondents stated they were prescribers of antibiotics, the majority of which were medical doctors (46%), then nurses (29%) and pharmacists (19%) (Supplementary Table S11). The majority of prescribers agreed they considered antibiotic resistance when treating a patient (92%), they have a key role to play in helping control antibiotic resistance (88%) and they are confident when making antibiotic-prescribing decisions (90%) (Table 2). Almost all prescribers were confident in the antibiotic guidelines available (96%), and they have easy access to those guidelines (94%).

Almost three-quarters (74%) of respondents agreed they feel supported not to prescribe antibiotics when they are not necessary. Over 20% of prescribers prescribed an antibiotic at

**Figure 5.** Reasons prescribers initiated antibiotic prescriptions when they would have preferred not to in the previous week, UK, 2019.

least once in the past week when they would have preferred not to (Figure 5). The reasons

**Table 2.** Responses from UK prescribers to the motivation statements.

#### *3.8. Summary Recommendations for Action from Stakeholder Workshop*

#### **4. Discussion**

This is the first UK-wide study assessing multidisciplinary HCWs' knowledge, attitudes and behaviour towards antibiotics, antibiotic use and resistance. As a sub-study of the multicountry EU/EEA survey, the UK results present the most comprehensive and detailed dataset for the UK so far, with responses from 2404 participants across a variety of age groups, professions and prescribing settings. All data were collected prior to the COVID-19 pandemic, providing insight into a population's baseline level prior to the widespread communication of prescribing measures that occurred throughout the pandemic. This analysis gives evidence for developing interventions targeted at HCWs, informing policy making, improving the reach and impact of public awareness campaigns and supporting HCWs with their antimicrobial stewardship.

The study exceeded its calculated quota sample by 74%, significantly increasing the generalisability and validity of the results at a country level. The UK constituted the largest proportion of respondents across the EU, equating to 13% of the total participants. However, it is worth noting that the majority of UK responses were from participants in England (50%) and Scotland (40%), limiting the direct application of these results to Northern Ireland and Wales and biasing the results to be more representative of Scotland in the context of the UK population. Volunteer bias risk is high in surveys; it is likely that those HCWs most interested in AMR completed the survey. Equally, it is possible that the wider prescribing population may not have the same level of interest and awareness of AMR. The authors also acknowledge the survey did not include the assessment of all elements of antimicrobial stewardship HCWs may utilise. Additional clinical decision and support tools, such as Electronic Health Records, and quality improvement initiatives, such as auditing, are valuable AMS strategies.

A key strength is the representation across all healthcare settings. In addition, the quota sample size was exceeded for key healthcare professional groups who prescribe, administer or dispense antibiotics such as physicians, nurses and pharmacists. [21]. In the UK, the largest groups of survey respondents were nurses and pharmacists, these two professions made up the highest percentage of the target sample size, at 175% and 462%, respectively (Supplementary Table S2). This emphasises the need to target future interventions and communications to these engaged groups and reinforces that they, along with physicians, can contribute to positive change in combating AMR. This differed to the EU/EEA in which physicians made up the greatest proportion of respondents, followed by nurses and pharmacists [16]. This is to be expected, as in mainland Europe, only medical doctors are able to prescribe.

The findings highlighted gaps in knowledge across all healthcare professional groups. Although HCWs understood the risk of side effects to the patient, fewer understood that antibiotic use increases a person's risk of AMR. Similarly, despite over 90% of HCWs understanding that healthy people can be colonised with antibiotic-resistant bacteria, one in five UK HCWs knew resistant bacteria can spread between people. It is important that prescribers understand the wider implications of AMR on patient outcomes. The positive results in the knowledge test correlate with earlier studies; in the United States,

Hamilton et al. found that 97% (*n* = 194) of nurse practitioners understood antibiotics can harm the patient and inappropriate use can cause resistance (97%) [11].

Overall, EU/EEA knowledge was stronger than the UK's regarding spread, but marginally weaker when it came to understanding a patient's increased risk of AMR. Future campaigns should consider including messages on the transmission of AMR, addressing the gap in knowledge identified through this study. National and local educational groups could also include these messages within their infection-related training materials.

Access to guidelines for managing infections was high in the UK (78%); however, fewer HCWs had access to the materials needed to provide advice and opportunities to provide that advice (68% and 62%, respectively). Improving opportunities to provide advice is a particular area of concern in the UK, as fewer UK respondents agreed with this statement in comparison to the EU/EEA as a whole. Increasing access to resources, as well as improving opportunities for HCWs to provide advice to patients on beneficial and judicious antibiotic use, are key to maximising HCWs' antimicrobial stewardship (AMS) capabilities. Intervention types should align with the behaviour change wheel [18] and focus on training, environmental restructuring, modelling exemplar behaviours and enablement [22] to produce durable development and improvement.

All HCWs can contribute to tackling AMR via good infection prevention and control practices; however, only 63.9% of respondents felt they had a key role in controlling AMR. As would be expected, the equivalent figure was higher in prescribers, where 88.4% felt they had a key role. Further engagement with HCWs should focus on empowering them in optimal AMS prescribing practices and reinforcing their vital role in tackling resistance. Educating HCWs on the wider context of One Health actions and impact may encourage their ensuing motivation for behaviour change, highlighting the importance prescribing behaviour can have on this global health challenge [23].

Findings from this study provide insight into the reasons why practitioners do not give AMS advice and are reinforced by the EU/EEA survey results. A lack of resources is the most frequently cited barrier (19% of respondents) to giving out advice. This can be addressed by implementing patient educational resources about antibiotics and resistance and making them easily accessible for practitioners. Resources should be accompanied by national and local campaigns to increase awareness and outline their purpose for use. These findings provide evidence of the need to further promotion and dissemination of available AMS resources such as TARGET (Treat Antibiotics Responsibly, Guidance, Education and Tools), EAAD/WAAW resources, When Should I Worry' patient brochure or 'Treating Your Infection' patient leaflet. More than half of respondents answered 'unsure' when asked if they were aware of or have used the TARGET resources; in a small evaluation of TARGET resources, participants (including HCWs) have reported these resources are useful, reinforcing the value of further dissemination [24]. A limitation of this study is that it is not known whether participants who had access to the resources were more likely to provide advice on antibiotics. It is also pertinent to understand barriers and enablers to their use. Insufficient time was cited as the second most common barrier to providing advice across both the UK and EU/EEA. This is concordant with the UK finding that only 62% of HCWs felt they had sufficient opportunity to provide advice on antibiotics (Table 1).

It is important to consider all barriers associated with prudent prescribing, taking into account the professional group, and investigate them further in order to best support HCWs to overcome these challenges. The fear of patient deterioration or complications was the foremost reason (34% of respondents), both in primary and secondary care settings, for issuing an antibiotic prescription, and uncertainty in diagnosis was the second most common reason (25%). These findings correlate with the literature; fear has been cited as a common barrier to tackling AMR amongst community healthcare providers and physicians, alongside patient pressure, time and systemic overworking [12,13,25,26].

Other factors to consider include consultation time constraints, prescriber–patient relationships and patient awareness and expectations in receiving antibiotic prescriptions. Further qualitative research is warranted to improve our understanding of these factors and implement useful and successful interventions.

International and national campaigns provide means through which to reach more population numbers. WAAW and EAAD managed to reach nearly half of the UK respondents, with 45% stating they were aware of WAAW, and 46% were aware of EAAD. Nationally, 76% of UK HCWs had seen or heard the KAW advert on TV or radio. Conversely, in answer to a separate question, only 36% of respondents stated they were aware of or had used KAW materials.

Tackling AMR requires engagement at individual, population and government levels. The Antibiotic Guardian (AG) initiative, of which more than half of the study cohort (53.7%) are aware of or have used, includes the proactive engagement of 'pledging' [26]. The evaluation of the AG campaign demonstrated an increased commitment of healthcare workers, scientists/educators and the public in tackling AMR, increased self-reported knowledge and changed self-reported behaviour, particularly among people with prior AMR awareness [27,28]. Pledging has been identified as an effective and inexpensive driver for behaviour change relating to antibiotic use [27]. It provides individuals with concrete actions and examples of how to tackle AMR and at the same time includes them in the collective movement to drive change.

The survey identified that Facebook was the most popular social media platform used by UK HCW respondents for professional use. This communication channel presents an opportunity to disseminate information and engage with HCWs. A significant proportion (44%) of participants did not use any of the social media platforms listed. In future surveys, it would be worth expanding communication efforts beyond social media channels to engage with participants in a more inclusive manner, ultimately increasing impact.

It is important that the UK considers the findings of this study and advocates for next steps and actions to tackle the public health threat of AMR. This study provides baseline data for policy makers on AMR awareness and AMS involvement within the HCW population. It would be insightful to undertake the survey in the wake of the COVID-19 pandemic, to help assess what, if any the impact pandemic may have had (with the consistent infection prevention and control measure messages), on HCW populations and their awareness of AMR and AMS. Moreover, conducting regular surveys to evaluate ongoing initiatives would be valuable in order to measure impacts and identify areas for improvement.

The implementation of actions at both national and local levels is imperative to changing practice and behaviour. The effectiveness of interventions on improving antibiotic prescribing depends on prescribing behaviours and on perceived and actual barriers to change. Multifaceted educational interventions occurring on multiple levels will only be effective after local barriers to change are addressed [29–31]. Educational, training or communications materials for HCWs in the UK should consider the findings of this study when developing content/curriculum and embed behaviour change strategies as part of developing interventions.

#### **5. Conclusions**

These findings strengthen our understanding of UK HCWs' knowledge, attitudes and behaviours towards antibiotics and antibiotic resistance and provide an evidence base for guiding future AMS activities, interventions and research priorities. The results highlight HCWs' comprehension of AMR; however, specific knowledge gaps across professional groups should be targeted in future educational initiatives. Training materials should address the risk of AMR spread and the impact this has for individuals and the public. Resources, initiatives and future campaigns should be promoted across a variety of social media platforms to maximise engagement with UK HCWs. Further evaluation is needed to identify the most effective method for communicating with practitioners that do not use social media professionally. The findings identify potential barriers faced by HCWs. Subsequent evaluation is needed of the barriers and enablers to inform future interventions

on improving awareness of and access to antibiotic resources, increasing the opportunity for HCWs to use these resources and supporting prescribers not to prescribe when they feel antibiotics are not needed. Future surveys should be undertaken to longitudinally inform and evaluate strategies in this field. Research on novel interventions should embed behaviour change strategies, aligning with the behaviour change wheel, to produce effective, long-lasting and positive behaviours relating to antibiotics and their use.

**Supplementary Materials:** The following supporting information can be downloaded at: https://www. mdpi.com/article/10.3390/antibiotics11081133/s1, Supplementary Material. Table S1: UK responses across the devolved administrations; Figure S1: Participation in the survey by region in England; Table S2: UK quota sample size and responses to the survey; Table S3: Percentage of UK respondents by profession; Table S4 Respondents' age, gender and professional setting; Table S5: Percentage of UK and EU/EEA respondents that use the different social media platforms; Figure S2: The percentage of respondents answering all seven knowledge test questions correctly - by profession; Figure S3a: Percentage of respondents answering question 5 correctly, by professional group; Figure S3b: Percentage of respondents answering question 6 correctly, by professional group; Table S6: Respondents answering all seven knowledge test questions correctly, by UK constituent; Table S7: Respondents answering the One Health knowledge question correctly; Table S8: Respondents answering the Hand Hygiene knowledge question correctly; Figure S4: Percentage of respondents who agree with the following motivation statements; Figure S5: Percentage of UK respondents agreeing to the motivation statements (by constituent); Table S9: The frequency of prescribing/administering/dispensing antibiotics during the last one week; Figure S6: Percentage of respondents that gave out resources or advice; Table S10: Barriers: Most common reasons why UK healthcare workers were unable to provide advice or resources to their patients in a one-week period; Figure S7: Percentage of respondents who agree with the campaign impact and effectiveness statements in the UK and EU/EEA; Figure S8: Percentage of respondents who agree with the campaign impact and effectiveness statements across the devolved administrations; Figure S9: Awareness of campaigns in a. the UK b. the EU/EEA; Figure S10: Perceived effectiveness of EAAD and WAAW in the UK; Figure S11: Awareness of campaigns, projects and platforms related to antibiotic use and AMR in the UK; Figure S12: Engagement with Antibiotic Guardian; Figure S13: Awareness of the Keep Antibiotics Working Campaign; Table S11: Professions of prescribers in the UK; Table S12: Setting of prescribers in the UK; Figure S14: Responses from UK prescribers to the motivation statements.

**Author Contributions:** Conceptualisation, D.A.-O. and S.H.; data curation, D.A.-O., E.U. and S.V.; formal analysis, E.C. and S.V.; funding acquisition, D.A.-O. and S.H.; methodology, D.A.-O., E.U., J.R. and S.H.; project administration, E.C., E.U. and S.V.; supervision, D.A.-O. and S.H.; writing—original draft, D.A.-O., E.C., E.U. and S.V.; writing—review and editing, D.A.-O., E.C., E.H., E.U., S.V., J.R. and S.H. All authors have read and agreed to the published version of the manuscript.

**Funding:** The survey was funded by the European Centre for Disease Prevention and Control (ECDC) through a specific service contract (ECD.8836) to Public Health England, London, United Kingdom. The analysis and interpretation of the findings was completed by the contractor.

**Institutional Review Board Statement:** The data for this study were extracted from and comply with the ethical statement for the research undertaken by Ashiru-Oredope et al. [16]. Informed consent was provided prior to participation. The original study was part of an evaluation of the EU EAAD communications campaign which commenced in 2008 and included significant input in development and distribution from the PAG. The PAG officially represented all participating countries and European professional groups and organisations.

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** Additional data from the study can be found via https://www.ecdc. europa.eu/en/publications-data/survey-healthcare-workers-knowledge-attitudes-and-behavioursantibiotics (accessed on 1 April 2021).

**Acknowledgments:** The authors would like to thank all healthcare workers and individuals who promoted the survey locally/nationally or via social media. The authors would also like to thank the ECDC Project Advisory Group: Reinhild Strauss (Austria); Vinciane Charlier, Samuel Coenen (Belgium); Miranda Serti´c, Marina Payerl-Pal (Croatia); Linos Hadjihannas, Costas A. Constantinou (Cyprus); Barbora Macková (Czech Republic); Lisa Bugge-Toft (Denmark); Pille Märtin, Mailis Hansen (Estonia); Outi Lyytikäinen, Jari Jalava (Finland); Anne Berger-Carbonne, Mélanie Colomb-Cotinat (France); Flora Kontopidou, Maria Foteinea (Greece); Martin Cormican, Audrey Lambourn (Ireland); Francesca Furiozzi, Michela Sabbatucci (Italy); El¯ına Dimin, a, Kate Vulane (Latvia); Virginija ¯ Kanapeckiene, Jolanta Kuklyt ˙ e (Lithuania); Peter Zarb, Michael A. Borg (Malta); Renske Eilers (the ˙ Netherlands); Harald Pors Muniz (Norway); Waleria Hryniewicz, Beata Mazi ´nska (Poland); Duarte Pedro De Sousa Tavares (Portugal); Livia Cioran, Alexandra Cucu (Romania); Eva Schreterova (Slovakia); Mitja Vrdelja, Maja Subelj (Slovenia); Rocío Bueno Parralo, Antonio López Navas (Spain); Agneta Andersson, Karin Carlin (Sweden); Jacqui Reilly, Diane Ashiru-Oredope (UK); Lea Pfefferle, Task Force on Antibiotics in Dentistry (Council of European Dentists); Petr Horák, Steffen Amann (European Association of Hospital Pharmacists); Andreas Trobisch, Lenneke Schrier (European Academy of Paediatrics); Tanguy Pinedo-Tora, Alyette Greiveldinger (European Dental Students' Association); Elena Carrara, Nico T. Mutters (European Committee on Infection Control); Charles Price (European Commission); Mathias Maucher (European Federation of Public Service Unions); Michele Calabrò (European Health Management Association); Pascal Garel, Laurie Andrieu (European Hospital and Healthcare Federation); Laura Alonso Irujo, María Santacreu García (European Joint Action on Antimicrobial Resistance and Healthcare-Associated Infections, EU-JAMRAI); Kitty Mohan, Sara Launio (European Junior Doctors Association); Orsolya Réka Süli (European Medical Students' Association); Ivana Silva (European Medicines Agency); Mervi Jokinen (European Midwives Association); Marta Simões, Ruben Viegas (European Pharmaceutical Students' Association); Ann Marie Borg, Sascha Marschang (European Public Health Alliance); Céline Pulcini (European Society of Clinical Microbiology and Infectious Diseases Study Group for Antimicrobial stewardship); Ber Oomen, Jeannette Verkerk (European Specialist Nurses Organisations); Ilaria Giannico, Paul Garassus (European Union of Private Hospitals); Roberto Bertollini, Melina Raso (Health First Europe); Tímea Rezi-Kató (MedTech Europe); Jan De Belie, Ilaria Passarani (Pharmaceutical Group of the European Union); Jacques de Haller, Carole Rouaud (Standing Committee of European Doctors); Jo Bosanquet, Wendy Nicholson (WHO Collaborating Centre for Nurses); Cristiana Salvi (WHO/Europe). The authors would also like to acknowledge individuals who contributed to the development of the survey tool or attended meetings of the Project Advisory Group, in particular: Jan Eyckmans, Herman Goossens, Anne Ingenbleek, Ann Vesporten (Belgium); Sven Pal, Edita Suši´c (Croatia); Gideon Ertner (Denmark); Katja Sibenberg (Finland); Alise Gramatniece, Aija Vilde (Latvia); Roxana Serban (Romania); Elizabeth Beech, Leah Jones, Lyndsey Patterson, Muhammad Sartaj, Katherine Le Bosquet, Enrique Castro-Sanchez, Yvonne Dailey, Joanne Bosanquet, Penny Greenwood, Ayoub Saei (United Kingdom); Ana Maria Navarro Tamayo (European Joint Action on Antimicrobial Resistance and Healthcare-Associated Infections, EU-JAMRAI); Miriam D'Ambrosio (Standing Committee of European Doctors); Danilo Lo Fo Wong (WHO/Europe). In addition, the authors would like to pay gratitude to temporary members of the core team, especially Ola Oloyede and Aleksa Dubanowicz. The authors also thank attendees of the ECDC UK Findings Workshop that took place in June 2020: Alicia Demirjian, Anna Sallis, Aoife Hendrick, Bharat Patel, Ceri Phillips, Cliodna McNulty, Donna Lecky, Jacqui Sneddon, Jordan Charlesworth, Kiran Loi, Leah Jones, Mohamed Sadak, Natalie Gold, Nicholas Reid, Philip Howard, Sally Weston Price, Susie Singleton and Viviana Finistrella.

**Conflicts of Interest:** The authors declare no conflict of interest.

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