Background

Antibiotics are substances that specifically target bacteria, as they can inhibit growth and even kill bacteria; hence, they are intended to treat and prevent bacterial infections [1,2,3]. Antibiotics are among the most commonly prescribed medications, especially for childhood illnesses, as in pediatric dentistry [4, 5]. However, the major contributors to outpatient visits are acute diarrhea, acute upper or lower respiratory infection, and viral infection with fever, indicating that only a small percentage of pediatric patients (< 20%) need antibiotic therapy [6]. On the other hand, the most common condition in pediatric patients who require antibiotic prescription is acute otitis media, as reported in the United States and Canada [7, 8]. While antibiotics are critical in healthcare, their usage in pediatric care, especially in developing countries, presents unique challenges. According to previous studies, antibiotics are responsible for 27% of medication-related pediatric medical errors and 19% of hazardous errors caused by systemic antibiotic use [9,10,11], especially those related to antibiotic dosing [5]. Antibiotic dosage is determined by taking into account a number of factors, including age, weight, and coexisting disorders [12, 13]. Furthermore, the lack of clinical trials on antibiotics for pediatric patients and the lack of new antibiotic pipelines have led to a paucity of high-level evidence [14, 15]. Antibiotic resistance has reached an alarming level worldwide, particularly in developing countries [16, 17]. The inappropriate use of antibiotics, particularly broad-spectrum antibiotics for these childhood diseases, has contributed largely to the evolution of antibiotic resistance [6], and this is the most serious problem worldwide [18]. Cultural, educational, behavioral, and socioeconomic factors are among the numerous factors that contribute to antibiotic resistance. Therefore, the exacerbation of antibiotic resistance must be clearly and deeply known by all members of the health care system, including pharmacists, and a plan must be presented for an effective strategy to improve antibiotic use and the creation of antibiotic supervision programs to prevent further spread of antibiotic resistance.

While many studies on the appropriate use and dosage of antibiotics for children have been undertaken in various regions of the world, relatively few studies have focused on Palestinian community pharmacists to assess this topic [5, 19,20,21,22,23,24]. This national study aimed to evaluate the knowledge of community pharmacists on the northern West Bank of Palestine on the appropriate use and dosing of antibiotics for pediatric patients. Overall, this study highlights the importance of increasing awareness campaigns to promote appropriate antibiotic use in pediatric patients. The results of this study may be valuable for policymakers and healthcare providers in developing local guidelines and interventions to improve appropriate antibiotic use.

Methods

Study design and setting

This was a cross-sectional questionnaire-based study that was conducted in Palestine from September 11, 2022, to March 27, 2023, targeting pharmacists working in community pharmacies. Participants were approached from 5 different cities, Nablus, Jenin, Tubas, Tulkarm, and Qalqilya, and from their respective villages and camps, which represent northern Palestine. The data were gathered through the use of a well-organized questionnaire distributed online. This online survey was administered via the SurveyMonkey platform and subsequently disseminated across various digital channels, including WhatsApp, Facebook Messenger, Facebook, and email. Due to logistical limitations, we opted for online data collection methods instead of in-person visits to specific districts. Notably, many other studies have also supported the use of a self-administered questionnaire survey method for data collection [6, 25, 26]. Approximately 10–15 min were needed to complete the questionnaire. The study protocol was approved by the Institutional Review Board (IRB) of An-Najah National University.

Sampling procedure

According to a previous study [27], there were 2350 pharmacists in Nablus, Jenin, Tubas, and Qalqilya. The Daniel formula was used [28]; n = Z2*P (1-P)/d2, where n = the calculated sample size for populations exceeding 10,000, z = 1.96 (95% CI), d = 0.05 (absolute precision as a margin of error), and P = 0.5 expected prevalence or response distribution. The sample size was 385 participants. However, since our population was less than 10,000 (N = 2,350), we adjusted this number using the adjusted sample equation; adjusted sample = n/(1 + (n/N)). The sample size needed was approximately 331, considering a 5% margin of error, a response of 50%, and a 95% confidence interval.

Questionnaire development

A thorough evaluation of relevant surveys was performed to identify potentially relevant questions for the questionnaire utilized in our study [5, 21, 26, 29,30,31,32,33,34,35,36,37]. A comprehensive review of the questionnaire was performed to validate the questions and ensure that the answers were correct. The questionnaire was subsequently sent to specialists with extensive research experience, including an infectious disease medical doctor, an infectious disease clinical pharmacist, and an academic pharmacy researcher. These experts conducted individual reviews of the questionnaire and made comments and modifications. The initial version of the questionnaire was adjusted based on their recommendations. Minor modifications were also made in the subsequent revisions until the final version was obtained. The infectious disease specialists provided correct answers. Finally, all specialists read the final edit and approved it.

Prior to the release of the survey, a pilot study of ten questionnaires was performed to analyze and clarify the questionnaire items. The questionnaire has four major components:

  • The first part contains questions regarding sociodemographic characteristics (gender, age, years of working, etc.).

  • The second part included questions assessing participants’ knowledge, practices, and attitudes toward antibiotic use and antimicrobial resistance.

  • The third part was composed of questions regarding a case scenario for antibiotic dosing and labeling of instructions.

  • The fourth part concentrates on evaluating the barriers and obstacles to the appropriate prescription and use of antibiotics, as well as the effects of sociodemographic factors on the knowledge of community pharmacists about appropriate antibiotic use in pediatrics.

Inclusion and exclusion criteria

The study included pharmacists in the northern West Bank (Jenin, Nablus, Tulkarm, Qalqilya, Tubas, and their villages and camps), provided that they were registered with Palestine Pharmacists Syndicate and working community pharmacies aged 23 years and older. The study excluded nonworking pharmacists and pharmacists working in pharmaceutical fields other than community pharmacies, such as hospital pharmacies, pharmaceutical factories, and medical representatives.

Statistical analysis

Data analysis was performed with IBM SPSS version 29. Descriptive analysis was used to summarize the data, including frequency and percentage for categorical variables and mean and median for continuous variables. The total knowledge score for antibiotics was calculated and ranged from zero to fifteen, where a score of zero indicated that all questions were answered incorrectly and a score of fifteen indicated that all questions were answered correctly. The pharmacists were then classified as knowledgeable or non-knowledgeable based on their total score. Non-knowledgeable pharmacists were those who answered fewer than eight questions correctly, while knowledgeable pharmacists were those who scored eight or more points. The Mann‒Whitney test was used for binary variables, the Kruskal‒Wallis test was used for variables with more than two groups to analyze the knowledge score, and a p value less than 0.05 was considered to indicate statistical significance.

Results

Sociodemographic characteristics of the study sample

Among the 301 community pharmacists who completed the questionnaire, the average age was 30.06 years, and the vast majority of the pharmacists were females (75.1%). Approximately half of them lived in the city (49.8%). In addition, 87.7% of them graduated from Palestinian universities, and more than half worked as pharmacy employees (67.4%). In addition, most of the participants had less than 5 years of experience (60.8%). All the details can be found in Table 1.

Table 1 Sociodemographic characteristics of the study sample
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Knowledge of community pharmacists in Palestine on antibiotics

The pharmacists’ knowledge about antibiotics is shown in Table 2. The results showed that 18.3% of the pharmacists still believed that antibiotics were effective against viruses. More than half of the pharmacists thought that antibiotics were effective for coughs lasting more than a week, and 61.8% answered that antibiotics were useful for killing germs. Only 67.8% knew that diarrhea did not improve faster with antibiotics.

Table 2 Knowledge of community pharmacists in Palestine about antibiotics
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Antibiotic resistance, according to more than 99% of the pharmacists in our study, occurs when bacteria develop various resistance mechanisms against the effects of antibiotics, and 92.1% of the pharmacists agreed that it can be very difficult to treat the infections they cause.

When azithromycin was used for acute bacterial pharyngitis, 93% of the pharmacists correctly answered that trimethoprim/sulfamethoxazole can be used for lower urinary tract infections. For the otitis and sinusitis scenarios, our findings showed that the majority of pharmacists (92.7% and 81.1%, respectively) correctly answered the use of amoxicillin/clavulanate and cefdinir as therapeutic options.

Practices of community pharmacists in Palestine toward pediatric antibiotics

A descriptive analysis of the practices of community pharmacists toward pediatric antibiotics is shown in Table 3. For example, adaptation to pediatric antibiotic prescriptions was rated as very good for 32.6% of pharmacists and weak for 3.7%. Regarding the recalculation of the dose written by the physician in the prescription of antibiotics for children, 30.6% were excellent, and 4.3% were weak. Furthermore, 34.9% of the patients were excellent, and 5.3% of them were weak in contacting the doctor when an inappropriate regimen (antibiotic dose/frequency is too high or too low) was noted. According to the analysis of the prescription scenario, 78% of the pharmacists gave instructions correctly, and 83% refused to fill prescriptions due to the wrong dosage (Table 4).

Table 3 Practices of community pharmacists in Palestine toward pediatric antibiotics
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Table 4 Prescription scenario
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Attitudes of pharmacists toward antibiotic use

As noted in Tables 5 and 95.7% of the pharmacists considered themselves responsible for informing and educating parents who requested antibiotics for their children without a prescription and who were probably not in need of antibiotic therapy. Furthermore, 97% of them agreed that the medicine-related counseling of community pharmacists was just as important as the recommendations of the physician. However, there is some variation, where 20.3% of pharmacists dispense antibiotics without prescriptions due to the demands of parents. Furthermore, 80.4% of the pharmacists believed that nonprescription dispensing of antibiotics was a public health risk, and 47.5% of them offered probiotics for patients purchasing prescribed antibiotics.

Table 5 Attitudes of pharmacists toward antibiotic use
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Barriers that prevent the appropriate prescription and use of antibiotics

According to the pharmacists, there were many barriers that could prevent appropriate antibiotic prescription and use, such as parents’ behavior with respect to antibiotic use (91.7%), physician malpractice with respect to prescribing antibiotics (88.7%), and parents’ pressure to prescribe antibiotics (87.3%), as illustrated in Table 6.

Table 6 Barriers that prevent the appropriate prescription and use of antibiotics
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The effects of sociodemographic factors on the knowledge of community pharmacists about appropriate antibiotic use in pediatrics

The analysis of sociodemographic factors affecting the knowledge of community pharmacists about antibiotics showed that age, position in the pharmacy, social status, and years of work were independently associated with the knowledge of community pharmacists about antibiotics. Age was positively associated with pharmacist knowledge, as pharmacists aged 45 years and older were more knowledgeable than those under 45 years (P value = 0.013). Additionally, position in the pharmacy had a positive association with pharmacists’ knowledge, and pharmacists who were employees were more knowledgeable than those who were employers (P value = 0.002). Furthermore, years of work experience were positively associated with pharmacist knowledge: pharmacists with 5 years of working experience were more knowledgeable than those with less than 5 years of working experience (P value = 0.001). The details are shown in Table 7.

Table 7 Knowledge of community pharmacists according to demographic characteristics
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Discussion

The current study revealed that community pharmacists were highly knowledgeable about the appropriate prescription and use of antibiotics (98%). While pharmacists may not serve as prescribers in many countries, knowledge about the appropriate selection of antibiotics is crucial. They play an important role in conducting interventions or providing recommendations to clinicians regarding the appropriate choice of drugs. Several studies have evaluated pharmacists’ beliefs that antibiotics are not effective at treating cold, flu, or cough. In Jordan, 56.1% of pharmacists believed that antibiotics would never treat cold, cough, or flu [38]; Zakaa El-din et al. reported that 10.4% of the respondents thought that antibiotics are helpful for sore throat and common colds [39], while in Catalonia, Spain, 34.8% of pharmacists dispensed antibiotics for sore throat complaints [40]. In our study, 80.1% of the pharmacists were against prescribing antibiotics for these indications. However, 61.8% of the pharmacists responded that antibiotics are effective at killing germs. This could be attributed to the fact that the term “germs” is generally used with antibiotics rather than specific bacteria [37]. This demonstrates the critical need for pharmacists to be more knowledgeable about antibiotic indications, and they should feel obligated to make patients aware of their misuse and the consequences of their actions.

Almost all the pharmacists (99%) in our study responded that the misuse of antibiotics led to antimicrobial resistance, whereas 79% of those in the Jordanian study [38] and another Palestinian study (92.1%) reported antimicrobial resistance [41]. The substantial increase in knowledge could be attributed to the fact that community pharmacists are well educated and have professional skills and training that allow them to provide the best health care services [34], as well as the fact that many patients seek medical advice directly from community pharmacies because they are faster and less expensive than doctor clinic visits are and because they are considered reliable and easy to contact healthcare providers [39, 42].

The level of practice in the current study was assessed by presenting one case scenario and six questions on the practices of community pharmacists in Palestine regarding pediatric antibiotics. Approximately 61.5% of community pharmacists correctly calculated the dose of amoxicillin, compared to 54% in Chicago [25]. The variability could be attributed to differences in study objectives and study populations (age groups, sample size), in addition to the fact that more than 99.9% of community pharmacies dispense amoxicillin and cephalexin over the counter, so they are familiar with the dosing [43].

Regarding the evaluation of the practices of community pharmacists in Palestine regarding pediatric antibiotics, 86.4% would consult physicians if they were uncertain about the appropriateness of antibiotic prescription. This finding is in agreement with the results of a study in Senegal (90.2%) [44] and greater than what was reported in the Jordanian study (53.5%) [38] as well as the study by Rehman et al. in Pakistan (32%) [45]. In Palestine, as in some developing countries, patients can obtain antibiotics from pharmacies without a prescription [27, 39]. In fact, because some participants do not refer to physicians due to poor physician response, this may reflect the necessity of strengthening interprofessional relationships between healthcare teams, most likely starting with university curricula. Pharmacists and other health care practitioners should collaborate in multidisciplinary teams to minimize antimicrobial irrationality and inappropriate use and hence antimicrobial resistance. Understanding how to develop relationships with caregivers can help change their attitudes and increase the acceptability of pharmacists who interfere with children’s antibiotic prescriptions. Caregivers seeking symptom relief may be more amenable to nonantibiotic options [46]. With respect to dosing considerations, 85% of the pharmacists recalculated the dose written by the physician before dispensing the antibiotic. Almost 93% of the pharmacists correctly answered the question on utilizing azithromycin for acute bacterial pharyngitis. Similarly, the use of a trimethoprim/sulfamethoxazole dosage for treating lower urinary tract infections was identified for 93% of the patients. Our knowledge rates were higher than those reported by Keewan et al. in their study in Jordan [5], where the largest number of community pharmacists (55.8%) properly answered the case of azithromycin dose in acute bacterial pharyngitis, while 15.7% of the pharmacists correctly answered the dosing of trimethoprim-sulfamethoxazole in lower urinary tract infection. To ensure the accurate dispensing of antibiotics for pediatric patients, double-checking could be implemented.

Approximately 98% of participants agreed that education about antibiotic use and antibiotic resistance should be more prominent during university education years, as concluded by studies in India [47], Trinidad and Tobago [48], and East Africa [49].

In our study, several factors exhibited statistically significant associations with pharmacist knowledge. These factors include younger age, employment status within a community pharmacy, and an accumulation of more than five years of professional experience. A study carried out in the West Bank, Palestine, demonstrated that women and those living in urban areas have higher knowledge scores [41]. On the other hand, it was discovered that pharmacist education, professional title, and years of experience had an impact on the pharmacist’s understanding of antimicrobial medications [50]. These findings highlight the importance of customizing antimicrobial stewardship programs to meet pharmacist requirements, taking into account sociodemographic differences. In addition, regarding the years spent working in the pharmacy, this association could be because pharmacists spend much time in the pharmacy, which means more time communicating with patients, prescriptions, and promotional representatives who scientifically explain their medications.

Several community pharmacists have reported barriers that can contribute to inappropriate antibiotic use in pediatrics. Among them, parental behavior and pressure to prescribe antibiotics (91.7% and 87.3%, respectively) were the barriers most frequently reported. This was followed by malpractice in antibiotic prescribing (88.7%). These findings were consistent with a study conducted in Lebanon in which pharmacists first blamed parents (90.1%), second-level physicians (72.8%) and third-level physicians (59.4%) for inappropriate antibiotic use and the emergence of antimicrobial resistance [37]. Furthermore, in Qatar, patients and practitioners, mainly physicians, play a role in shaping barriers to appropriate antibiotics [26]. In contrast, unfounded assumptions about the efficacy of antibiotics by health professionals, as well as an exaggeration of parents’ desire for medications, may be the key contributing cause of antibiotic overprescription for the common cold in Korea [51]. This would support the need for antibiotic stewardship programs and effective behavior change programs that are getting off to a good start to optimize antibiotic prescription.

Strengths and limitations

The strengths of this study include the high number of responses and the scenario design that community pharmacists are more likely to encounter; moreover, the study succeeded in containing clear questions about practices and attitudes toward antibiotic use. This is the first study in the West Bank, Palestine, to discuss antibiotic use and dosing among pediatric patients. However, there are a few limitations. For example, using the cross-sectional design in this study prevented us from interpreting the causality of significant associations. In addition, the current study is based on the real practice of pharmacists with respect to antibiotic use, so the pharmacist might check a reference or consult a colleague when answering the cases, which could lead to an overestimation of pharmacist knowledge. Additionally, the research in question employed an online survey featuring a convenience sample. Consequently, there is potential for bias, as the survey’s reach may be confined to individuals with internet connectivity. Furthermore, the utilization of the convenience-oriented snowball sampling method raises concerns about the representativeness of this study’s findings in relation to the entirety of Palestinian pharmacies. The smaller sample size and the use of online surveys may limit the generalizability of the study’s findings to the entire population of pharmacists in the northern West Bank of Palestine. However, the final sample size remains statistically robust for analysis considering the population size. Further research with a larger sample size and a more representative recruitment strategy could strengthen the generalizability of the results. The final constraint pertains to the study’s design, which adopts a cross-sectional analysis. This design impedes the identification of causation and limits the generalizability of the study’s findings.

Conclusions

This study aimed to assess the level of knowledge possessed by community pharmacy professionals with regard to the correct use of antibiotics by pediatric patients. The investigation revealed that a significant proportion of community pharmacists demonstrated a commendable understanding of the appropriate usage of antibiotics. Furthermore, the outcomes indicated a positive correlation between pharmacists’ knowledge and their years of professional experience and social status. This observation lends support to the proposition that the acquisition of professional expertise and the quality of training contribute to the provision of enhanced healthcare services. The findings derived from this investigation provide valuable insights into the proper use of antibiotics in pediatric care. Nevertheless, it is worth noting that the results of this study may not be readily generalizable to a broader population. Consequently, it is advisable to implement ongoing educational programs, including interactive workshops and lectures led by infectious disease specialists, under the coordination and support of the Palestinian Pharmacist Syndicate and awareness campaigns aimed at enhancing the prescription and utilization of antibiotics among community pharmacists. This recommendation is especially pertinent in light of the continuously evolving guidelines and evolving information within this domain.

Future perspectives

This study emphasizes the need for continuous educational and awareness efforts to improve the understanding of proper antibiotic use and prescription guidelines among children. Due to the high frequency of mistakes in pharmaceuticals, especially related to dosage, providing effective treatments for children is crucial for reducing this problem and improving patient safety standards. Future research efforts may focus on developing and implementing educational programs specifically designed to enhance the knowledge and skills of community pharmacists in this field. Moreover, there is a significant advantage in educating parents and caregivers on the prudent use of antibiotics and the possible risks associated with prescription inconsistencies. This can be achieved through the use of educational materials, such as brochures distributed in pediatric clinics. In addition, community pharmacists should take the lead in ensuring that parents understand the instructions, risks, and proper use of antibiotics. Furthermore, future research may aim to examine the impact of these treatments on the prescription practices of pharmacists, patient health outcomes, and healthcare costs. In conclusion, the results of this study have the potential to impact policy choices and inspire practical improvements in the quality of care for children while limiting the risk of prescription mistakes.