Knowledge, Attitude, and Practices of Mothers Working as Nurses Toward Multidrug-Resistant: Impact of an Educational Program in Neonatal Intensive Care Unit

Introduction

The proliferation of multidrug-resistant bacteria (MDROs) in healthcare settings is problematic because infected neonates are harder to treat and have worse outcomes.¹ Neonates who contract MDROs have greater morbidity and mortality rates and are especially susceptible to chronic infections caused by MDROs.² Worldwide, an estimated 3 million cases of newborn sepsis are reported annually, with up to 570,000 sepsis-related deaths; a large number of these deaths are related to the ineffectiveness of the current antibiotics.³ Antibiotics are administered to up to 40% of neonates admitted to neonatal intensive care unit (NICUs), and 90% of these patients are expected to be exposed to antibiotics during their stay in the unit.⁴ Because there is a noticed or established requirement for experimental or particular treatment of MDR infections, several of these kinds of antibiotics are given without a prescription. Infection risk is significant for neonatal intensive care unit (NICU) admissions, particularly those born prematurely, for a variety of causes, such as immunocompromised due to an underdeveloped immune response, prolonged hospital stays, and frequent application of invasive medical equipment and drugs.⁵ Over the past two decades in patient care settings, some multidrug-resistant gram-negative bacteria have become much more common, particularly in neonatal and pediatric units.⁶ Based on recent literature, neonates require exceptional care.⁷ The NICU is the most therapeutic setting suitable for the care of neonates with critical conditions.⁵ Antibiotics are the most routinely prescribed drugs in NICUs related to the high incidence of morbidity and mortality of newborns in NICUs, clinical symptoms of infection are still limited yield.⁸ Antibiotics are essential in treating bacterial diseases that could cause severe medication reactions.⁹ However, when antibiotics are overused, they contribute to MDROs which serve as an obstacle to risk neonates.¹⁰ Antibiotic treatment duration is a major medical concern that depends on neonatologist suggestions, risks, and effects.⁸

The way mother working as healthcare workers behave may have an impact on how neonates are affected.¹¹ These nurses are the largest and the most important team of healthcare professionals who come into contact with people of all ages, including neonates.¹² They play an important part in disease prevention and control such as infectious diseases.¹³ In a hospital, nurses are responsible for all antibiotic process. This vital behavior affects treatment success, the development of MDROs and the antibiotic contact between nurses and the environment.^14,15 For example, the disposal of unused IV antibiotics could violate the best practices or standards set by regulators. However, nurses disposed of antibiotics in hospital sinks.^16,17 The presence of these germs has been linked to infections related to the healthcare sector, as has the prevalence of MDROs in wastewater.^17,18 Antibiotic overuse contributes to MDROs and can act as a signal to neonates’ elevated risk. In addition to the improper agent(s), the dose, frequency, and mode of administration, as well as the wrong culture collection of specimens and analysis norms increase multidrug resistance in clinical outcomes of high-risk neonates.^16,19 These nurses must enhance their communication skills with prescribers and pharmacists. According to Olans et al,²⁰ education was deemed necessary to promote knowledge regarding the link between antibiotic resistance and antibiotic use to practice the correct protocol for culture-taking, and to aid in communication, to enhance knowledge, attitude, and practice to prevent MDROs. In all healthcare setting nurses lack knowledge, attitudes, and best practices to deal with antibiotics regarding MDROs specifically and the corresponding infection control procedures.^16,21 Furthermore, endeavors to prevent infections caused by MDROs should encompass not only antibiotic usage and implementing measures to halt MDROs transmission but also enhancing our comprehension of MDROs transmission, particularly within hospital environments. A thorough examination of nurses’ knowledge, attitudes, and practices regarding antibiotic prescription, usage, and resistance is imperative. Significantly, a substantial proportion of respondents recognizes antibiotic resistance as a notable public health issue in their context, yet disparities exist in knowledge and practices.

There is also a notable inclination toward prescribing antibiotics in cases of doubt of infection. Concerns arise regarding the influence of patient demands, with a considerable percentage admitting to prescribing antibiotics due to patient insistence or to maintaining patient trust.²² Inappropriate antibiotic usage is influenced by various factors that contribute to the misuse and overuse of these medications in addition to one significant factor that is physicians’ nonadherence to treatment guidelines, which may stem from a lack of awareness or disregard for established protocols, so the nurse’s role is to adhere to the physician to follow the protocol.²³ Additionally, insufficient knowledge of MDROs (nurses) plays a role in this global problem. Fear of clinical failure and external pressures, such as influence from patient demands for antibiotics regardless of necessity, also contribute to the problem. Furthermore, self-prescribing exacerbates the issue by bypassing professional medical guidance, and all of these challenges addressed by Malhotra et al²³ were found to contribute to antibiotic resistance. It is crucial to provide guidelines and timely, comprehensive information to address this concern and this needs an educational program.²⁴ Neonatal nurses need to feel confident in their practice, as a lack of understanding of MDROs can impact the quality of care, professional-patient relationships, and interprofessional interactions. In light of this, the author conducted this study to investigate the impact of educational programs on improving nurses’ knowledge, attitude, and practice regarding antibiotic use and the prevention of antibiotic resistance.

Method

The quasi-experimental design was employed, deemed feasible for simulating real-world studies in neutral settings. Educators need to ascertain whether the intervention instigated a shift in outcomes, rather than delving into the causative factors behind the change.²⁵ This study used two groups, the first group was called the educational group, and the second group was called the non-educational group. The educational group was evaluated two times. Initially, nurses working in the Neonatal Intensive Care Unit (NICU) underwent assessment for their knowledge, attitudes, and practices concerning MDROs (pre-test, X1). Subsequently, they were reassessed for knowledge and attitudes regarding MDROs immediately after receiving the educational intervention developed by the research team (post-test, X2), followed by an assessment of their practices through a self-reported questionnaire two weeks after the intervention. The non-educational group underwent two assessments of their knowledge, attitudes, and practices regarding MDROs. Firstly, nurses were evaluated (pre-test, X1), followed by a second evaluation without any intervention (post-test, X2). The educational group consisted of nurses from Al-Basheer Hospital. Control hospitals were Raya Hospital, Moath Bin Jabal Hospital, Rahma Hospital, and al-Abdali Hospital. The sample size for the two nonequivalent group pre-post design with a power level of 0.8, a significant alpha level of 0.05, and a moderate effect size of 0.25 based on G power was 80 participants. Adding a 15% attrition rate for 184 participants. A convenient sample technique was utilized to recruit the participants. A convenient sample technique was utilized to recruit the 184 participants. The criteria for eligibility were mothers who working as nurses in NICU and were able to participate in the study.

The instrument comprises four sections, including demographic data, nurses’ knowledge of MDROs, nurses’ attitudes toward MDROs, and nurses’ practices regarding MDROs, all adapted from Lalithabai et al.²⁶ The demographic section encompasses gender, age, hospital of employment, education level, primary role, years of general experience, years of NICU experience, and completion of an antibiotic handling educational course within the last six months. The section on nurses’ knowledge of MDROs, also adapted from Lalithabai et al,²⁶ comprises a self-descriptive scale consisting of 20 statements categorized into three groups: six statements regarding antibiotic information, six statements concerning antibiotic resistance, and eight statements addressing prevention of multidrug-resistant organisms. The scale demonstrated a Cronbach’s Alpha of 0.65. Each statement is a multiple-choice question with four options, only one of which is correct. Scores below 10 (50%) are categorized as indicating “poor knowledge”, scores between 10 (50%) and 15 (75%) indicate “good knowledge”, and scores exceeding 15 (75%) indicate “excellent knowledge”. The section on nurses’ attitudes toward MDROs, also from Lalithabai et al,²⁶ comprises 15 items measured on a 5-point Likert scale. Scores below 30 (50%) indicate “poor attitude”, scores between 30 (50%) and 42 (70%) indicate “moderate attitude”, and scores exceeding 54 (90%) indicate “good attitudes”. The reliability, assessed by Cronbach’s alpha, was 0.7, and validity was confirmed by five experts.

The section on nurses’ practices toward MDROs consists of 14 items divided into two categories: nine items on antimicrobial delivery practices adapted from El Baida & Mina (2022), consisting of nine yes/no questions, and one multiple-choice question. The Cronbach’s Alpha for this section was 0.65. The second category comprises five items on advice given to patients regarding antimicrobial usage, adapted from Balliram et al,²⁷ assessed through yes/no questions. This instrument, developed by Balliram et al,²⁷ categorizes an overall practice score of less than or equal to 6 as indicating ”poor practice” and a score exceeding 6 as indicating ”good practice”.

The educational program aimed to enrich the knowledge, attitude, and practices of nurses in preventing the harm caused by MDROs at al-Basheer Hospital. The program, integrated into the nurses’ educational group, adopted the educational module from the Minnesota Department of Health (MDH) in the United States. This module defined antibiotic resistance, explained the development of antibiotic-resistant organisms, highlighted the impact on patients, families, and neonatal care facilities, and provided actionable steps to manage their development and spread. Guided by the WHO Curriculum Guide for Nurses on Antimicrobial Resistance and CDC recommendations, the program covered theoretical aspects such as distinguishing between antibiotic and antimicrobial resistance, inappropriate antibiotic prescription scenarios, antibiotic initiation, timeouts, allergy history, adverse effects, culture result reconciliation, the definition of antibiotic misuse, and associated complications.

The practical component encompassed infection control procedures in NICU, identification of broad-spectrum antibiotic use, recognizing opportunities for oral antibiotics over intravenous administration, observation and identification of potential adverse events, timing of administering antibiotics to high-risk neonates, ensuring cultures are obtained before starting antibiotics, promoting antibiotic time-outs, offering appropriate discharge assistance and follow-up instructions, antibiotic reconciliation, and educating caregivers. These educational sessions were conducted by the research assistant who hold a master degree in nursing and received a training about MDROs education using PowerPoint presentations in both English and Arabic languages, with distribution facilitated through the WhatsApp application. The sessions were complemented with supporting videos to enhance the understanding of the presented material. The data collection was conducted between August 2023 to November 2023.

Data Analysis

The Statistical Package of Social Sciences (SPSS) version 28 was used, the data was checked before statistical analysis. The means, median, and standard deviation were used. Furthermore, the bivariate chi-square test was employed to compare the baseline and after education statements of the nurses in the educational and non-educational groups.

Ethical Considerations

This study was approved from Deanship of Research in Jordan University of Science and Technology IRB (348-2023). The written informed consent was signed from all participants in the study that informs them of all their rights and expectations from the study. The guidelines outlined in the Declaration of Helsinki were followed.

Results

Description of the Demographic Differences Between the Two Group

Table 1 presents a comparison of socio-demographic and professional characteristics between the educational and non-educational groups according to the hospital name. The distribution of participants across hospitals shows significant differences (X2 = 168.00, df = 4, p < 0.001).

Table 1 Comparison of the Nurses’ Socio-Demographic and Professional Characteristics Between the Two Groups of Nurses. N=168

Nurses’ Knowledges of MDROs

The t-test did not show a significantly difference between educational and non-educational groups (t = −1.439, df = 167, p = 0.152) during pre-test period. They were similar in knowledge and participants demonstrated relatively low levels of knowledge. The t-test revealed a significant improvement in post-education knowledge scores (M = 16.94) compared to pre-education scores (M=12.9929 (t = 40.119, df = 83, p <0.001). This means educational programs effectively enhance nurses’ knowledge of various antibiotic resistance concepts. Following the educational intervention, participants in the educational group exhibited substantial improvements in accurately defining antibiotics, identifying side effects, grasping antibiotic resistance, and understanding appropriate antibiotic usage. The remarkable enhancement in overall knowledge underscores the efficacy of the educational program in enriching participants’ understanding of critical antibiotic-related concepts. The findings revealed a significant increase in nurses’ responses in the educational group across all items except two (items 6 and 14). For further insights into the comparison of nurses’ knowledge-related questions between the pretest and post-test in the educational group, see Table 2.

Table 2 Comparison of Nurses’ Knowledge Toward Antibiotic Use and Prevention of Antibiotic Resistance in the Pre-Post Educational Time

Nurses’ Attitudes Towards MDROs

The overall mean attitude scores for both groups suggest no significant difference between the educational (46.64) and non-educational groups (46.32). This indicates that there is no significant difference between both groups in attitude before applying to educational program groups (t = 104, df = 167, p = 0.56). The t-test to compare the means of attitude between pre-education and post-education. The overall attitude scores indicate a noteworthy improvement post-education, with the mean scores increasing from pretest 46.64 to posttest 58.45. The total attitude shift is statistically significant (t = 104.23, df = 83, p < 0.001). See Table 3

Table 3 Comparison of Nurses’ Attitudes Toward Antibiotic Resistance in the Post-Pre-Educational Time

Nurses’ Practice Toward MDROs

The chi-square test was conducted to compare the practice in the pretest and post-test for the educational group items and also between two groups at baseline. The t-test was used to compare the mean score between two groups. The overall practice data suggest that education has positively influenced neonatal nurses’ practices related to antibiotic usage with mean before education 11 and 12.7 (p = 0.38, t = 149.11) after education. For more details about the comparison of nurses’ questions of practice at the Pre-Posttest of the educational group in Table 4.

Table 4 Comparison of Nurse’s Practice Questions in the Post-Pre-Education Time

Correlation Between Nurses’ Knowledge, Attitudes, and Practice Toward MDROs

There is a significant correlation between post-knowledge and post-attitude (r = 0.251, p = 0.021), suggesting that as post-education knowledge increases, post-education attitude tends to be enhanced. This finding could imply that learning more about antibiotics and resistance is related to a more critical or cautious attitude in some circumstances. See Table 5

Table 5 Bivariate Pearson’s Correlations Between Attitude, Knowledge, and Nurses’ Practice Toward Antibiotic Use and Prevention of Antibiotics in the Intervention Group

Discussion

To best of our knowledge, this is one of the few studies that conducted in Jordan that aims to determine the impact of educational program on improving knowledge, attitude, and practice among nurses in NICU. Our study showed that the intervention group was statistically significant in the post-test in attitude and nurse knowledge with positive changes in neonatal nursing practice toward MDROs before and after the educational interventions, and there was a notable improvement in overall knowledge scores, indicating a significant increase in post-education knowledge compared to pre-education scores. Likewise, the overall attitude scores showed a significant enhancement post-education, with mean scores increasing from the pretest to the posttest. Additionally, concerning overall practice, the data suggest that education has positively impacted neonatal nurses’ practices regarding antibiotic usage, as evidenced by the mean scores before and after education. Similarly, three studies conducted in Asia to examine the result of an educational program on nurses’ attitudes, knowledge, and practice toward the MDROs.^28–30

Firstly, Lim and Bang²⁹ in South Korea, findings demonstrated that NICU nurses’ knowledge and practice regarding MDROs infection management had improved as a result of their participation in the educational program. This study highlights the importance of education and training in improving infection prevention practices between health professionals to stop and inhibit the growth of multidrug-resistant organisms. Secondly, Qadir et al³⁰ in Pakistan found a consistent decrease in rates for MDROs in 12 months following the intervention period. Third, Galal et al²⁸ in Cairo, found that the nurses’ knowledge and attitudes about infection prevention significantly improved after the infection control program was provided by the hospital. Also, the knowledge among the nurses in the post-intervention phase on different types of nosocomial bacterial infections, infection risk classifications, infection control strategies, and different kinds of hand washing was significantly higher.

Two studies conducted in the United States for examining nurses’ attitudes, knowledge, and practice related MDROs fields.^31,32 Firstly, Polisetty et al³¹ showed that nurses had improved attitudes and beliefs toward antibiotic stewardship, they have a better understanding of the importance of the effects of antibiotic resistance and safe antibiotic use. Wilson et al³² results demonstrated that the online course significantly improved nurses’ knowledge and attitudes toward antimicrobial programs after the class, the mean knowledge scores rose from 75% to 86%.

Our study found that post-attitude, post-knowledge, and post-practice were found to be correlated to each other’s. These results were similar to the studies in literature. Two studies conducted in Asia investigated the correlation between nurses’ knowledge, practices, and attitudes in the field of neonatal MDROs.^33,34 They discovered that the majority of nurses reported adherence to preventive and control measures, exhibiting positive attitudes and practices. Additionally, a positive correlation was observed between attitude and practice. Nair et al³³ conducted research in India, where nurses’ knowledge was found to be at 63.4%, attitude at 79.9%, and practice at 75.5%. However, a significant finding was the inconsistency between knowledge and practice, as participants demonstrated an understanding of appropriate antibiotic application attitudes but failed to translate this understanding into practice. In contrast, two studies in Asia regarding the relationship between neonatal nurses’ knowledge, practices, and attitudes regarding MDROs.^13,26,35 Lalithabai et al²⁶ in Saudi Arabia found no statistically significant correlation between knowledge and attitude about MDROs, as well as a small relationship between the score for attitude and the overall knowledge score. Secondly, Hayat et al³⁵ in Pakistan found that although there was a lack of knowledge of MDROs the majority of nurses were seen to have a good attitude toward hospital-based MDROs. Moreover, two studies conducted in Africa regarding the relationship between the practices, attitudes, and knowledge of neonatal nurses towards MDROs.^36,37 Firstly, Sanneh et al³⁷ in Gambia found several of the nurses, who were shown to have less knowledge of antibiotic resistance while having a positive attitude and practice. Secondly, Dramowski et al³⁶ conducted a study in South Africa and found that there was a practice gap between nurses’ knowledge levels and the apparent increase in compliance across the reported research. The practical gap that requires being addressed to consistently stop the spread of infection in the setting of a pandemic is highlighted by the noted limitations in nurses’ compliance and knowledge.

Our study found that the nurses in the intervention group had a significantly higher mean knowledge of antibiotic use at the post-intervention group score compared to the nurses who had not received the intervention course. Our results were improved in response to educational programs not related to any other factors. Similarly, Polisetty et al³¹ in the United States showed that knowledge and attitude about medications and resistant antibiotics and demographic characteristics such as age, gender, and the number of years of experience are correlated. A study conducted in Western Europe in France by Vaillant et al³⁸ found five factors were strongly associated with more knowledge: being employed in a university hospital; age classes 26–35 years and 36–45 years; medical professional status, having experience in an intensive care unit and having received training in the management of antibiotic resistance. Additionally, Toska & Geitona³⁹ in Greece found a statistically significant connection among the nurses’ gender, educational level, and age, as well as the kind of hospital and professional experience, and their assessments of MDROs and illogical prescriptions. The type of hospital was also linked to views of MDROs and antibiotic use for common children’s illnesses. In contrast, four studies conducted in Asia regarding predictors of attitude, knowledge, and practices among neonatal nurses regarding the MDROs.^34,35,40,41 Firstly, Abuhammad et al⁴² in Jordan found that the degree of knowledge was significantly related to the nurses’ age, education, and number of years of experience. Secondly, a study in Pakistan by Hayat et al³⁵ found a significant correlation between age and years of experience and knowledge of antibiotic resistance. Thirdly, Zhou & Chen³⁴ in China found that knowledge regarding MDROs infection prevention and control was strongly connected positively with many parameters such as hospital grade, employment position, and emphasis on establishing and avoiding MDROs infections with the female gender. Similar factors, as well as regular supervision and training, were found to be connected to attitude.

These factors, as well as age group and employment as nosocomial infection control personnel, regular supervision, and the number of training sessions per year, were also associated with self-reported practice.^44–46 Additionally, there was a study conducted by Ogoina et al⁴³ in Africa in Nigeria that found that overall, there was a strong relationship between age, years of experience, and antibiotic resistance knowledge. Also, a study found that there were factors influencing practice including consistent medical staff turnover, an absence of “pediatric competent” nurses and doctors, lower senior healthcare coverage after hours, and time constraints in emergency departments. Many recent studies found that the appropriate practice regarding antibiotic use could decrease the MDRO problems specially in healthcare setting.

Implications

The results of this paper regarding the impacts of MRDOs education program provide neonatal mothers working as nurses with knowledge, attitude, and improve practice relying on evidence-based data as a basic core to implement high efficiency and quality of skills in clinical practice (providers cannot practice what they do not know) and reflect on the struggles of MDROs on neonates that are caused by malpractice, poor knowledge, negative attitude regarding the prevention of MDROs and prevent the consequences of problems that may lead to an increase in morbidity and mortality. These initiatives can be translated into neonatal nurses and lead to a fundamental change in the standard prevention of MDROs programs in Jordan by the integration of education into regular and daily basis treatment in NICU.

Conclusion

With an increasing need for neonatal nurse roles to avoid MDROs in neonates with serious medical conditions and the proven positive impact of MDROs programs on neonatal nurses, it became necessary to improve the nurses’ knowledge, attitude, and practice regarding MDROs. It provides a good proof that the MDROs educational program is advantageous in enhancing nurse knowledge and attitudes toward MDROs prevention, as well as delivering an effective instructional program for nurses, based on the outcomes of this study.