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Nursing Students’ Knowledge and Awareness of Antibiotic Use, Resistance and Stewardship: A Descriptive Cross-Sectional Study

Rábano Blanco, Andrea; Domínguez Martís, Eva María; Mosteiro Miguéns, Diego Gabriel; Freire-Garabal Núñez, Manuel; Novío Mallón, Silvia

Abstract

Antibiotic resistance is an emerging worldwide concern with serious repercussions in terms of morbi-mortality. Bearing in mind that the inadequate use of antibiotics, by healthcare staff as well as by the general population, is one of its main causes, a multidisciplinary approach is required to try to combat it. The aim of the present study was to determine nursing students’ knowledge and awareness of antibiotic use, resistance and stewardship. A cross-sectional design was used. A total of 578 nursing students from the University of Santiago de Compostela (Spain), ≥18 years old of both sexes were invited to complete the Spanish version of the questionnaire “Knowledge and awareness of the use, resistance and administration of antibiotics” between February and April 2019. Students had a low level of knowledge about antibiotics, 4.1 (CI95% = 3.4–4.8), especially in relation to antibiotic resistance. As the students were aware of this deficiency, the majority affirmed (>90%) that the current curriculum of nursing degree should have more training on antibiotics and infection control. Nursing staff play an important role in the rational use of antibiotics and as teachers of patients, so their training could be key in fighting antibiotic resistance.

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antibiotics Article Nursing Students’ Knowledge and Awareness of Antibiotic Use, Resistance and Stewardship: A Descriptive Cross-Sectional Study Andrea Rábano-Blanco 1, Eva María Domínguez-Martís2, Diego Gabriel Mosteiro-Miguéns 3, Manuel Freire-Garabal 4and Silvia Novío5,* 1Galician Public Health Care Service, Milladoiro, Ames, 15895 A Coruña, Spain; andr[email protected] 2Galician Public Health Care Service, Health Care Centre of Ordes, Ordes, 15680 A Coruña, Spain; [email protected] 3Badalona Serveis Assistencials, Family and Community Nursing, Health Care Centre of Morera-Pomar, 08915 Badalona, Spain; [email protected] 4School of Medicine, University of Santiago de Compostela, 15782 A Coruña, Spain; manuel.freir[email protected] 5Department of Psiquiatry, Radiology, Public Health, Nursing and Medicine, School of Medicine and Dentistry, University of Santiago de Compostela, 15782 A Coruña, Spain *Correspondence: [email protected]; Tel.: +34-881-812-374 Received: 10 October 2019; Accepted: 28 October 2019; Published: 30 October 2019   Abstract: Antibiotic resistance is an emerging worldwide concern with serious repercussions in terms of morbi-mortality. Bearing in mind that the inadequate use of antibiotics, by healthcare staffas well as by the general population, is one of its main causes, a multidisciplinary approach is required to try to combat it. The aim of the present study was to determine nursing students’ knowledge and awareness of antibiotic use, resistance and stewardship. A cross-sectional design was used. A total of 578 nursing students from the University of Santiago de Compostela (Spain), ≥ 18 years old of both sexes were invited to complete the Spanish version of the questionnaire “Knowledge and awareness of the use, resistance and administration of antibiotics” between February and April 2019. Students had a low level of knowledge about antibiotics, 4.1 (CI95% =3.4–4.8), especially in relation to antibiotic resistance. As the students were aware of this deficiency, the majority affirmed (>90%) that the current curriculum of nursing degree should have more training on antibiotics and infection control. Nursing staffplay an important role in the rational use of antibiotics and as teachers of patients, so their training could be key in fighting antibiotic resistance. Keywords: Anti-bacterial agents; awareness; drug resistance; knowledge; nursing; students 1. Introduction Antibiotics are medicines that fight bacterial infections. They can save lives if they are used correctly, but nowadays antibiotic resistance has become a real problem [ 1 ]. Infections by resistant microorganisms do not respond to treatment, so the duration of the disease is prolonged, and the risk of death increases. Moreover, if the treatment fails or if the response to treatment is slow, the patient is contagious for longer, which increases the likelihood of resistant microorganisms being transmitted to other people [2]. The emergence of antibiotic resistance is a natural biological phenomenon, and even though numerous factors have been identified as the cause of this, such as clustering and overcrowding or increased elderly population [ 2 ], one of the most important factors is the inadequate use of antibiotics [ 3 ], a very worrying situation especially for healthcare professionals with high rate of antibiotic prescription such as primary care dentists [ 4 ]. According to the World Health Organization (WHO), inadequate Antibiotics 2019,8, 203; doi:10.3390/antibiotics8040203 www.mdpi.com/journal/antibiotics Antibiotics 2019,8, 203 2 of 18 use of antibiotics includes the prescription of inappropriate antibiotics for a brief time, in low or insufficient doses and/or for diseases for which they are not indicated; likewise, excessive therapeutic dosage regimens are also considered inadequate uses of antibiotics [ 5 ]. In the specific case of Spain, the consumption of antibiotics for outpatients is above the European average, and in hospitals their prescription is increasing [6]. The inadequate use of antibiotics can be encouraged by self-medication, by the implementation of permissive policies in terms of regulation of the use of these drugs, by the relationship between the healthcare professional and the patient or by the knowledge and attitudes that one has towards them [ 7 , 8 ]. Regarding the latter, while it is true that a poor knowledge or negative attitude towards antibiotics leads inevitably to bad clinical practice, practical skills are not always a reflection of knowledge, a situation known as “theory–practice gap” [9]. To date, the studies which have evaluated the training that healthcare students have about infectious diseases, antimicrobial resistance and safe use of antibiotics have been mainly carried out in students of medicine[ 7 , 9 ]andpharmacy[ 10 – 12 ], besides students from other disciplines suchasdentistry [ 13 ]. However, taking into account that the control of antibiotic resistance requires a multidisciplinary approach, and that nursing staff play a key role in the rational use of antibiotics, as teachers of patients, and as future drug prescribers in our country, the training of nurses could have an important impact in reducing the incidence of antibiotic resistance. Thus, the objective of this paper has been to determine the nursing students’ knowledge and awareness of antibiotic use, resistance and stewardship. 2. Results 2.1. Description of Sample A total of 578 students of the Degree of Nursing from the University of Santiago de Compostela (152 of the first year, 133 of the second year, 145 of the third year and 148 of the fourth year) were invited to participate in the study, with a response rate of 59% (66% of the first year, 85% of the second year, 52% of the third year and 36% of the fourth year). Table 1shows the demographic characteristics of the participants. Most were women, <25 years old, without antibiotics training prior entering nursing but with family members/close friends working in health-related fields. The students’ favourite practice area to develop their professional activity was, in order of frequency: Emergency, Intensive Care Unit (ICU) and Reanimation Unit (RU); Pediatric nursing and Obstetric-gynecologic nursing. 2.2. Knowledge and Awareness Regarding Antibiotic Use, Resistance and Stewardship The answers to questions about students’ general knowledge (questions 8–19) and specific knowledge and awareness of antibiotics use, resistance and stewardship (questions 24–40) are shown in Table 2. In general, the students had good general knowledge of antibiotics; however, the aspects where there was a greater lack of knowledge were the following: cefotaxime is a cephalosporin (question 10) and antibiotics cannot treat influenza (question 19). On the contrary, the students showed a wide lack of knowledge in terms of antibiotic resistance, despite that 94.5% of the students stated they had heard about antibiotic resistance (question 20), and 45.2% that they had discussed antibiotic resistance topics during the nursing degree (question 21). The questions with poorer results (<25% of correct answers) were: antibiotic resistance is a natural phenomenon (question 29), beta-lactamase is an enzyme produced by bacteria that can break down aminoglycosides (question 33) and bacteria may acquire efflux pumps that extrude the antibiotic from the cell (question 34). The overall median knowledge score (general and specific knowledge) was low (4.2 and 95% confidence interval 3.4–4.8), despite the fact that the scores improved during the degree (Table 2). On the contrary, no statistically significant differences were found between male and female students, or between students with or without family members/close friends working in health-related fields (Figure 1). Antibiotics 2019,8, 203 3 of 18 Table 1. Baseline characteristics of the study’s participants. All the results were expressed as n (%). Characteristics Programme First-Year Second-Year Third-Year Fourth-Year DK/NO % of the Total Sex Male 12 (22.2%) 19 (35.2%) 14 (25.9%) 9 (16.7%) 0 (0%) 54 (15.7%) Female 88 (30.4%) 94 (32.5%) 61 (21.1%) 45 (15.6%) 1 (0.3%) 289 (84.3%) Age <20 82 (51.9%) 73 (46.2%) 2 (1.3%) 0 (0%) 1 (0.6%) 158 (46.1%) 20-25 12 (7.3%) 35 (21.2%) 68 (41.2%) 50 (30.3%) 0 (0%) 165 (48.1%) >25 6 (31.6%) 5 (26.3%) 5 (26.3%) 3 (15.8%) 0 (0%) 19 (5.5%) DK/NO 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 1 (0.3%) Time living in Spain <3 2 (28.6%) 2 (28.6%) 3 (42.9%) 0 (0%) 0 (0%) 7 (2%) 3-6 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) >6 97 (29.3%) 108 (32.6%) 71 (21.5%) 54 (16.3%) 1 (0.3%) 331 (96.5%) DK/NO 1 (20%) 3 (60%) 1 (20%) 0 (0%) 0 (0%) 5 (1.5%) Practice area considered Community nursing 10 (16.9%) 8 (13.6%) 16 (27.1%) 25 (42.4%) 0 (0%) 59 (17.2%) Pediatric nursing 39 (27.5%) 43 (30.3%) 42 (29.6%) 18 (12.7%) 0 (0%) 142 (41.4%) Obstetric-gynecologic nursing 32 (26.4%) 38 (31.4%) 35 (28.9%) 16 (13.2%) 0 (0%) 121 (35.3%) Mental health nursing 17 (29.3%) 15 (25.9%) 15 (25.9%) 11 (19%) 0 (0%) 58 (16.9%) Occupational nursing 3 (30%) 2 (20%) 1 (10%) 4 (40%) 0 (0%) 10 (2.9%) Geriatric nursing 4 (12.9%) 9 (29%) 8 (25.8%) 10 (32.3%) 0 (0%) 31 (9%) Surgical-medical nursing 39 (38.6%) 35 (34.7%) 17 (16.8%) 10 (9.9%) 0 (0%) 101 (29.4%) Emergency, ICU and RU 55 (31.8%) 56 (32.4%) 34 (19.7%) 28 (16.2%) 0 (0%) 173 (50.4%) Teaching 9 (20.5%) 16 (36.4%) 10 (22.7%) 9 (20.5%) 0 (0%) 44 (12.8%) Other 1 (11.1%) 0 (0%) 6 (66.7%) 2 (22.2%) 0 (0%) 9 (2.6%) I have not decided yet 22 (28.6%) 28 (36.4%) 16 (20.8%) 10 (13%) 1 (1.3%) 77 (22.4%) Students with antibiotics training prior entering nursing faculty Yes 20 (48.8%) 7 (17.1%) 8 (19.5%) 6 (14.6%) 0 (0%) 41 (12%) No 80 (26.5%) 106 (35.1%) 67 (22.2%) 48 (15.9%) 1 (0.3%) 302 (88%) Students with family members/close friends working in health-related fields Yes 69 (33.8%) 60 (29.4%) 39 (19.1%) 35 (17.2%) 1 (0.5%) 204 (59.5%) No 31 (22.5%) 52 (37.7%) 36 (26.1%) 19 (13.8%) 0 (0%) 138 (40.2%) DK/NO 0 (0%) 1 (100%) 0 (0%) 0 (0%) 0 (0%) 1 (0.3%) Abbreviations: DK/NO. Do not know/no opinion; ICU. Intensive Care Unit; RU. Reanimation Unit. Antibiotics 2019,8, 203 4 of 18 Table 2. General and specific knowledge and awareness of antibiotics. All the results were expressed as n (%), except the variable OKS, which was presented as median and confidence interval. The correct answers have been highlighted in bold. Question (Q) Programme First-Year Second-Year Third-Year Fourth-Year DK/NO % of the Total p Q8: Amoxicillin is an antibiotic Disagree 2 (66.7%) 1 (33.3%) 0 (0%) 0 (0%) 0 (0%) 3 (0.9%) >0.05 Not sure 39 (81.3%) 7 (14.6%) 2 (4.2%) 0 (0%) 0 (0%) 48 (4%) Agree 59 (20.2%) 105 (36%) 73 (25%) 54 (18.5%) 1 (0.3%) 292 (85.1%) Q9: Aspirin is an antibiotic Disagree 92 (28.9%) 99 (31.1%) 74 (23.3%) 53 (16.7%) 0 (0%) 318 (92.7%) >0.05 Not sure 4 (22.2%) 13 (72.2%) 1 (5.6%) 0 (0%) 0 (0%) 18 (5.2%) Agree 4 (66.7%) 1 (16.7%) 0 (0%) 1 (16.7%) 0 (0%) 6 (1.7%) DK/NO 0 (0%) 0 (0%) 0 (0%) 0 (0%) 1 (100%) 1 (0.3%) Q10: Cefotaxime is a cephalosporin Disagree 1 (25%) 1 (25%) 1 (25%) 1 (25%) 0 (0%) 4 (1.2%) >0.05 Not sure 95 (38.3%) 95 (38.3%) 39 (15.7%) 18 (7.3%) 1 (0.4%) 248 (72.3%) Agree 4 (4.4%) 17 (18.9%) 35 (38.9%) 34 (37.8%) 0 (0%) 90 (26.2%) DK/NO 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 1 (0.3%) Q11:Antibiotics are useful for bacterial infections Disagree 4 (57.1%) 2 (28.6%) 0 (0%) 0 (0%) 1 (14.3%) 7 (2%) >0.05 Not sure 5 (62.5%) 2 (25%) 0 (0%) 1 (12.5%) 0 (0%) 8 (2.3%) Agree 91 (27.8%) 108 (33%) 75 (22.9%) 53 (16.2%) 0 (0%) 327 (95.3%) DK/NO 0 (0%) 1 (100%) 0 (0%) 0 (0%) 0 (0%) 1 (0.3%) Q12: Antibiotics are useful for viral infections Disagree 78 (27%) 95 (32.9%) 67 (23.2%) 49 (17%) 0 (0%) 289 (84.3%) >0.05 Not sure 10 (35.7%) 13 (46.4%) 4 (14.3%) 0 (0%) 1 (3.6%) 28 (8.2%) Agree 12 (46.2%) 5 (19.2%) 4 (15.4%) 5 (19.2%) 0 (0%) 26 (7.6%) Q13: Antibiotics are indicated to reduce any kind of pain and inflammation Disagree 64 (24.7%) 81 (31.3%) 68 (26.3%) 46 (17.8%) 0 (0%) 259 (75.5%) >0.05 Not sure 13 (32.5%) 17 (42.5%) 6 (15%) 3 (7.5%) 1 (2.5%) 40 (11.7%) Agree 23 (53.5%) 15 (34.9%) 1 (2.3%) 4 (9.3%) 0 (0%) 43 (12.5%) DK/NO 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 1 (0.3%) Antibiotics 2019,8, 203 5 of 18 Table 2. Cont. Question (Q) Programme First-Year Second-Year Third-Year Fourth-Year DK/NO % of the Total p Q14: Antibiotics can cause secondary infections after killing good bacteria present in our organism Disagree 6 (31.6%) 6 (31.6%) 3 (15.8%) 4 (21.1%) 0 (0%) 19 (5.5%) >0.05 Not sure 30 (39%) 21 (27.3%) 16 (20.8%) 10 (13%) 0 (0%) 77 (22.4%) Agree 64 (25.9%) 86 (34.8%) 56 (22.7%) 40 (16.2%) 1 (0.4%) 247 (72%) Q15: Antibiotics can cause allergic reactions Disagree 1 (50%) 0 (0%) 0 (0%) 1 (50%) 0 (0%) 2 (0.6%) >0.05 Not sure 11 (35.5%) 12 (38.7%) 6 (19.4%) 2 (6.5%) 0 (0%) 31 (9%) Agree 88 (28.4%) 101 (32.6%) 69 (22.3%) 51 (16.5) 1 (0.3%) 310 (90.4%) Q16: Patients may stop the use of antibiotics as soon as they start feeling better Disagree 88 (28.4%) 105 (33.9%) 66 (21.3%) 50 (16.1%) 1 (0.3%) 310 (90.4%) >0.05 Not sure 7 (41.2%) 6 (35.3%) 3 (17.6%) 1 (5.9%) 0 (0%) 17 (5%) Agree 4 (28.6%) 2 (14.3%) 6 (42.9%) 2 (14.3%) 0 (0%) 14 (4.1%) DK/NO 1 (50%) 0 (0%) 0 (0%) 1 (50%) 0 (0%) 2 (0.6%) Q17: Colds and coughs should always be treated with antibiotics as patients will recover more quickly Disagree 92 (28.4%) 103 (31.8%) 74 (22.8%) 54 (16.7%) 1 (0.3%) 324 (94.5%) >0.05 Not sure 8 (42.1%) 10 (52.6%) 1 (5.3%) 0 (0%) 0 (0%) 19 (5.5%) Agree 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) Q18: Antibiotics should always be prescribed as preventive measures to fight against future infections Disagree 92 (30.7%) 89 (29.7%) 67 (22.3%) 51 (17%) 1 (0.3%) 300 (87.5%) >0.05 Not sure 6 (21.4%) 19 (67.9%) 2 (7.1%) 1 (3.6%) 0 (0%) 28 (8.2%) Agree 2 (14.3%) 5 (35.7%) 5 (35.7%) 2 (14.3%) 0 (0%) 14 (4.1%) DK/NO 0 (0%) 0 (0%) 1 (100%) 0 (0%) 0 (0%) 1 (0.3%) Q19: Antibiotics cannot treat influenza Disagree 19 (26.4%) 24 (33.3%) 16 (22.2%) 13 (18.1%) 0 (0%) 72 (21%) >0.05 Not sure 27 (40.3%) 26 (38.8%) 6 (9%) 8 (11.9%) 0 (0%) 67 (19.5%) Agree 54 (26.6%) 63 (31%) 53 (26.1%) 32 (15.8%) 1 (0.5%) 203 (59.2%) DK/NO 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 1 (0.3%) Q24: Antibiotic resistance happens when a bacterium loses its sensitivity to an antibiotic Disagree 6 (40%) 4 (26.7%) 4 (26.7%) 0 (0%) 1 (6.7%) 15 (4.4%) <0.05 * Not sure 16 (44.4%) 8 (22.2%) 8 (22.2%) 4 (11.1%) 0 (0%) 36 (10.5%) Agree 77 (26.6%) 101 (34.8%) 63 (21.7%) 49 (16.9%) 0 (0%) 290 (84.5%) DK/NO 1 (50%) 0 (0%) 0 (0%) 1 (50%) 0 (0%) 2 (0.6%) Antibiotics 2019,8, 203 6 of 18 Table 2. Cont. Question (Q) Programme First-Year Second-Year Third-Year Fourth-Year DK/NO % of the Total p Q25: Inappropriate use of antibiotics causes antibiotic resistance Disagree 2 (66.7%) 0 (0%) 1 (33.3%) 0 (0%) 0 (0%) 3 (0.9%) <0.05 * Not sure 14 (56%) 8 (32%) 2 (8%) 1 (4%) 0 (0%) 25 (7.3%) Agree 84 (26.8%) 105 (33.5%) 72 (23%) 51 (16.3%) 1 (0.3%) 313 (91.3%) DK/NO 0 (0%) 0 (0%) 0 (0%) 2 (100%) 0 (0%) 2 (0.6%) Q26: Prescribing broad-spectrum antibiotics increases antibiotics resistance Disagree 2 (11.1%) 6 (33.3%) 6 (33.3%) 4 (22.2%) 0 (0%) 18 (5.2%) <0.05 * Not sure 50 (33.8%) 61 (41.2%) 22 (14.9%) 14 (9.5%) 1 (0.7%) 148 (43.1%) Agree 48 (27.3%) 46 (26.1%) 47 (26.7%) 35 (19.9%) 0 (0%) 176 (51.3%) DK/NO 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 1 (0.3%) Q27: Poor infection control practices by healthcare professionals cause spread of antibiotic resistance Disagree 2 (12.5%) 7 (43.8%) 6 (37.5%) 1 (6.3%) 0 (0%) 16 (4.7%) <0.05 * Not sure 43 (47.8%) 30 (33.3%) 12 (13.3%) 4 (4.4%) 1 (1.1%) 90 (26.2%) Agree 55 (23.5%) 75 (32.1%) 57 (24.4%) 47 (20.1%) 0 (0%) 234 (68.2%) DK/NO 0 (0%) 1 (33.3%) 0 (0%) 2 (66.7%) 0 (0%) 3 (0.9%) Q28: Antibiotics are overused nationally and internationally in healthcare Disagree 3 (60%) 1 (20%) 1 (20%) 0 (0%) 0 (0%) 5 (1.5%) >0.05 Not sure 24 (37.5%) 24 (37.5%) 10 (15.6%) 6 (9.4%) 0 (0%) 64 (18.7%) Agree 73 (26.7%) 88 (32.3%) 64 (23.4%) 47 (17.2%) 1 (0.4%) 273 (79.6%) DK/NO 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 1 (0.3%) Q29: Appropriate use of antibiotics can cause antibiotic resistance Disagree 60 (30.5%) 65 (33%) 45 (22.8%) 27 (13.7%) 0 (0%) 197 (57.4%) <0.05 * Not sure 18 (27.3%) 29 (43.9%) 11 (16.7%) 8 (12.1%) 0 (0%) 66 (19.2%) Agree 20 (26%) 19 (24.7%) 19 (24.7%) 18 (23.4%) 1 (1.3%) 77 (22.4%) DK/NO 2 (66.7%) 0 (0%) 0 (0%) 1 (33.3%) 0 (0%) 3 (0.9%) Q30: Antibiotic stewardship is a phenomenon for which a bacterium gains resistance to an antibiotic Disagree 65 (29.1%) 74 (33.2%) 47 (21.1%) 36 (16.1%) 1 (0.4%) 223 (65%) >0.05 Not sure 26 (34.2%) 25 (32.9%) 17 (22.4%) 8 (10.5%) 0 (0%) 76 (22.2%) Agree 9 (20. 9%) 14 (32.6%) 11 (25.6%) 9 (20.9%) 0 (0%) 43 (12.5%) DK/NO 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 1 (0.3%) Antibiotics 2019,8, 203 7 of 18 Table 2. Cont. Question (Q) Programme First-Year Second-Year Third-Year Fourth-Year DK/NO % of the Total p Q31: Exposure to antibiotics appears to be the principal risk factor for appearance of antibiotic-resistant bacteria Disagree 8 (36.4%) 7 (31.8%) 4 (18.2%) 3 (13.6%) 0 (0%) 22 (6.4%) >0.05 Not sure 39 (34.2%) 38 (33.3%) 22 (19.3%) 14 (12.3%) 1 (0.9%) 114 (33.2%) Agree 53 (25.9%) 68 (33.2%) 49 (23.9%) 35 (17.1%) 0 (0%) 205 (59.8%) DK/NO 0 (0%) 0 (0%) 0 (0%) 2 (100%) 0 (0%) 2 (0.6%) Q32: Antibiotic resistance can be minimized by using narrow-spectrum therapy after identification and susceptibility testing of infectious bacteria Disagree 2 (25%) 0 (0%) 4 (50%) 2 (25%) 0 (0%) 8 (2.3%) <0.05 * Not sure 60 (39.7%) 51 (33.8%) 21 (13.9%) 18 (11.9%) 1 (0.7%) 151 (44%) Agree 37 (20.3%) 62 (34.1%) 50 (27.5%) 33 (18.1%) 0 (0%) 182 (53.1%) DK/NO 1 (50%) 0 (0%) 0 (0%) 1 (50%) 0 (0%) 2 (0.6%) Q33: Beta-lactamase is an enzyme produced by bacteria that can break down aminoglycosides Disagree 0 (0%) 1 (100%) 0 (0%) 0 (0%) 0 (0%) 1 (0.3%) <0.05 * Not sure 97 (31.4%) 106 (34.3%) 64 (20.7%) 41 (13.3%) 1 (0.3%) 309 (90.1%) Agree 3 (9.7%) 5 (16.1%) 11 (35.5%) 12 (38.7%) 0 (0%) 31 (9%) DK/NO 0 (0%) 1 (50%) 0 (0%) 1 (50%) 0 (0%) 2 (0.6%) Q34. Bacteria may acquire efflux pumps that extrude the antibiotic from the cell Disagree 2 (33.3%) 2 (33.3%) 1 (16.7%) 1 (16.7%) 0 (0%) 6 (1.7%) >0.05 Not sure 86 (29.6%) 99 (34%) 66 (22.7%) 39 (13.4%) 1 (0.3%) 291 (84.8%) Agree 12 (27.3%) 11 (25%) 8 (18.2%) 13 (29.5%) 0 (0%) 44 (12.8%) DK/NO 0 (0%) 1 (50%) 0 (0%) 1 (50%) 0 (0%) 2 (0.6%) Q35: Use of antibiotics in livestock production and agriculture contributes to antibiotic resistance Disagree 2 (33.3%) 1 (16.7%) 1 (16.7%) 2 (33.3%) 0 (0%) 6 (1.7%) >0.05 Not sure 43 (38.1%) 29 (25.7%) 25 (22.1%) 15 (13.3%) 1 (0.9%) 113 (32.9%) Agree 55 (24.9%) 82 (37.1%) 48 (21.7%) 36 (16.3%) 0 (0%) 221 (64.4%) DK/NO 0 (0%) 1 (33.3%) 1 (33.3%) 1 (33.3%) 0 (0%) 3 (0.9%) Q36. Improving techniques for bacterial diagnostics will allow combating antibiotic resistance Disagree 1 (25%) 1 (25%) 1 (25%) 1 (255) 0 (0%) 4 (1.2%) <0.05 * Not sure 17 (47.2%) 12 (33.3%) 4 (11.1%) 3 (8.3%) 0 (0%) 36 (10.5%) Agree 82 (27.4%) 99 (33.1%) 70 (23.4%) 48 (16.1%) 0 (0%) 299 (87.2%) DK/NO 0 (0%) 1 (25%) 0 (0%) 2 (50%) 1 (25%) 4 (1.2%) Antibiotics 2019,8, 203 8 of 18 Table 2. Cont. Question (Q) Programme First-Year Second-Year Third-Year Fourth-Year DK/NO % of the Total p Q38: Today’s research will be sufficient to meet the future needs for new antibiotics Disagree 50 (27.3%) 61 (33.3%) 42 (23%) 30 (16.4%) 0 (0%) 183 (53.4%) >0.05 Not sure 34 (33%) 31 (30.1%) 21 (20.4%) 17 (16.5%) 0 (0%) 103 (30%) Agree 16 (28.6%) 21 (37.5%) 12 (21.4%) 6 (10.7%) 1 (1.8%) 56 (16.3%) DK/NO 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 1 (0.3%) Q39: Antibiotic resistance will be a greater clinical problem later in my nursing career than it is today Disagree 1 (20%) 3 (60%) 1 (20%) 0 (0%) 0 (0%) 5 (1.5%) >0.05 Not sure 8 (32%) 8 (32%) 8 (32%) 1 (4%) 0 (0%) 25 (7.3%) Agree 91 (29.3%) 101 (32.5%) 66 (21.2%) 52 (16.7%) 1 (0.3%) 311 (90.7%) DK/NO 0 (0%) 1 (50%) 0 (0%) 1 (50%) 0 (0%) 2 (0.6%) Q40: Formal teaching on proper usage of antibiotics among healthcare students may minimize the phenomena of antibiotic resistance Disagree 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 1 (0.3%) >0.05 Not sure 5 (33.3%) 6 (40%) 0 (0%) 4 (26.7%) 0 (0%) 15 (4.4%) Agree 95 (29.3%) 105 (32.4%) 75 (23.1%) 48 (14.8%) 1 (0.3%) 324 (94.5%) DK/NO 0 (0%) 2 (66.7%) 0 (0%) 1 (33.3%) 0 (0%) 3 (0.9%) OKS 3.8 (3.4-4.5) 4.1 (3.4-4.8) 4.5 (3.8-5.2) 4.8 (4.1-5.2) 3.4 (3.4-3.4) 4.1 (3.4-4.8) <0.001 * The overall knowledge score (OKS) was determined according to what has been explained in “Data processing and statistical analysis”. Intergroup differences were analyzed using the Kruskal–Wallis test. * Significant differences (p<0.05). Abbreviations: OKS. Overall knowledge score; DK/NO. Do not know/no opinion. Antibiotics 2019,8, 203 9 of 18 Antibiotics 2019, 8, x 7 of 16 Q39: Antibiotic resistance will be a greater clinical problem later in my nursing career than it is today Disagree 1 (20%) 3 (60%) 1 (20%) 0 (0%) 0 (0%) 5 (1.5%) >0.05 Not sure 8 (32%) 8 (32%) 8 (32%) 1 (4%) 0 (0%) 25 (7.3%) Agree 91 (29.3%) 101 (32.5%) 66 (21.2%) 52 (16.7%) 1 (0.3%) 311 (90.7%) DK/NO 0 (0%) 1 (50%) 0 (0%) 1 (50%) 0 (0%) 2 (0.6%) Q40: Formal teaching on proper usage of antibiotics among healthcare students may minimize the phenomena of antibiotic resistance Disagree 0 (0%) 0 (0%) 0 (0%) 1 (100%) 0 (0%) 1 (0.3%) >0.05 Not sure 5 (33.3%) 6 (40%) 0 (0%) 4 (26.7%) 0 (0%) 15 (4.4%) Agree 95 (29.3%) 105 (32.4%) 75 (23.1%) 48 (14.8%) 1 (0.3%) 324 (94.5%) DK/NO 0 (0%) 2 (66.7%) 0 (0%) 1 (33.3%) 0 (0%) 3 (0.9%) OKS 3.8 (3.4-4.5) 4.1 (3.4-4.8) 4.5 (3.8-5.2) 4.8 (4.1-5.2) 3.4 (3.4-3.4) 4.1 (3.4-4.8) <0.001* The overall knowledge score (OKS) was determined according to what has been explained in “Data processing and statistical analysis”. Intergroup differences were analyzed using the Kruskal–Wallis test. *Significant differences (p < 0.05). Abbreviations: OKS. Overall knowledge score; DK/NO. Do not know/no opinion. Figure 1. Overall knowledge score (OKS) in accordance with the sex and the existence of family members/close friends working in health-related fields. The overall knowledge score (OKS) was determined according to what has been explained in “Data processing and statistical analysis”. Intergroup differences were analysed using the Mann–Whitney U test. No significant differences were observed (p > 0.05). Figure 1. Overall knowledge score (OKS) in accordance with the sex and the existence of family members/close friends working in health-related fields. The overall knowledge score (OKS) was determined according to what has been explained in “Data processing and statistical analysis”. Intergroup differences were analysed using the Mann–Whitney U test. No significant differences were observed (p>0.05). Antibiotics 2019,8, 203 16 of 18 Supplementary Materials: The following are available online at http://www.mdpi.com/2079-6382/8/4/203/s1, Questionnaire: Cuestionario sobre conocimiento y conciencia de los estudiantes de Grado de Enfermer í a sobre el uso, resistencia y administración de antibióticos. Author Contributions: Conceptualization, A.R.-B. and S.N.; Data curation, A.R.-B., E.M.D.-M., D.G.M.-M. and M.F.-G.; Formal analysis, A.R.-B. and S.N.; Investigation, A.R.-B. and S.N.; Methodology, A.R.-B., E.M.D.-M., D.G.M.-M., M.F.-G. and S.N.; Project administration, A.R.-B. and S.N.; Supervision, A.R.-B. and S.N.; Validation, E.M.D.-M., D.G.M.-M., M.F.-G. and S.N.; Visualization, D.G.M.-M. and S.N.; Writing – original draft, A.R.-B., D.G.M.-M. and S.N.; Writing – review & editing, A.R.-B., E.M.D.-M., M.F.-G. and S.N. Funding: This research received no external funding. 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