Antibiotic Misuse during the COVID-19 Pandemic in Lebanon: A Cross-Sectional Study

: Background: Over the past 100 years, the discovery of antibiotics is regarded as one of the most significant advances in medical research and has saved millions of lives. However, the emergence of antimicrobial-resistant bacteria has significantly reduced the efficacy of antibiotics against infectious disorders. Antimicrobial resistance is mostly caused by antibiotic misuse for conditions that may be treated with self-care. During the COVID-19 pandemic, antibiotic use has been out of control among the general population. Aim: The objective of this study is to investigate the prevalence of antibiotic misuse during the COVID-19 pandemic in Lebanon. Methods: In January 2024, a descriptive cross-sectional study was conducted amongst students registered at the Islamic University of Lebanon. Individuals who have been infected with COVID-19 at least once were eligible for the study and were selected by a non-random snowball sampling technique. Descriptive and quantitative analyses were performed using SPSS 21. Results: Out of the 478 participants who completed the questionnaire, 40.2% ( n = 192) received antibiotics during the COVID-19 infection. A physician’s prescription is mentioned by some participants (51%, n = 98), followed by a pharmacist’s (23.4%, n = 45), self-taken (14.5%, n = 28), and others as family or friends (10.9%, n = 21). Moreover, 59.3% ( n = 114) of the respondents respected the antibiotic therapy’s rules, and 40.6% ( n = 78) discontinued taking the antibiotic when they felt better. Conclusion: Our results showed that participants were likely to show unsatisfactory compliance and to use non-prescribed antibiotics. Campaigns are urgently needed to promote appropriate antibiotic use.


Introduction
Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), which caused coronavirus disease 2019 (COVID- 19), has aroused widespread alarm due to the infection's rapid international spread and the clinical spectrum of the inflammatory sickness, which ranges from moderate to severe and resulted in death and multi-organ failure [1,2].The World Health Organization (WHO) declared COVID-19 a global pandemic in March 2020 [3].
The management of critically ill patients has been made possible by the following publications of guidelines on the management of the condition, particularly the use of steroids.Although infection management has received significant attention, the guidelines initially placed little focus on antibiotics due to a lack of adequate data.When COVID-19 was first discovered in Wuhan in December 2019, more than 90% of hospitalized patients received antibiotics despite the lack of convincing bacterial infection proof [4].Secondary bacterial problems associated with moderate and severe pneumonia cases might develop from COVID-19 infections and can be successfully treated with antibiotics; thus, antibiotics are not advised for all COVID-19 patients [5,6].The WHO guidelines issued a strict warning against administering antibiotics in such situations and reported that the massive rise in antibiotic resistance is primarily attributable to the inappropriate use of antibiotics, including the prescription of unnecessary antibiotics or the use of antibiotics with an overly broad spectrum and the wrong dosage or duration [7,8].
Studies have shown that there has been a comparable rise in antibiotic usage with the growth in infectious illnesses, despite the fact that antibiotics neither treat nor prevent viral infections, including COVID-19 [9,10].One of these studies reported that almost 80% of patients receiving antibiotics had no COVID-19 infection and were taking them ineffectively in an effort to stop the illness.Furthermore, even though only a small percentage (15%) of COVID-19 patients who were badly afflicted experienced bacterial co-infection, necessitating the need to start antibiotics, 75% of them ultimately received antibiotics [11].Social media's ability to spread panic and the fact that there is no recognized treatment for COVID-19-infected patients are both factors that helped to drastically increase the prevalence of self-treatment with medicine [12].
Unfortunately, self-treatment with medicine is on the rise across all societies globally, with some societies reporting prevalence rates of over 90% [13].It has been shown that selfmedicating with antibiotics can result in serious health issues, such as negative side effects, therapeutic failure, and, most importantly, antibiotic resistance [14,15].The prevalence of self-treatment with medicine was as high as 82%, with 20% to 50% of antibiotics being misused, according to a systematic analysis that evaluated antibiotics consumption outside of authorized healthcare facilities in low-and middle-income countries in the Middle East [16].There is limited published literature on antibiotic misuse during COVID-19 among the Lebanese population.This study aims to investigate the prevalence of antibiotic misuse during the pandemic in Lebanon.

Study Design and Participants
This cross-sectional research was carried out in January 2024.The Islamic University of Lebanon extended an invitation to all enrolled students to take part in this study.Participants in the study had to have had at least one COVID-19 infection.The goal was a non-random sample.The snowball method was used to recruit students in two phases.During the initial phase, all enrolled students at the university's several campuses (Beirut, Baalbek, Tyre, Mount Lebanon) received an online questionnaire from the administrative or IT department.The students were encouraged to complete the questionnaire and share it with their families and community.Using the sample size calculator "Raosoft", with a margin of error of 5%, confidence level of 95%, response distribution of 50%, and supposing a population size of 20,000, the sample size must be a minimum of 377 participants.

Instrument
The questionnaire was divided into three sections and contained 31 items: the participants' sociodemographic information, lifestyle and past medical history, and antibioticrelated healthcare-seeking behaviors (Supplementary Data: questionnaire).Information on gender, age, education level, working field, monthly income, BMI, smoking, and medical history was gathered through sociodemographic questions.The behaviors included using antibiotics for self-treatment, using prescription drugs, reasons for antibiotic usage, and whether the COVID-19 vaccine was taken.Participants were also asked to list the antibiotic brands or chemicals that they had used.The questions on antibiotic use behaviors were adapted from previous studies [17].The questionnaire was pre-tested on a pilot population (n = 15) to determine whether the data would provide reliable information, then translated into Arabic, then backtranslated into English to validate the translation.Students were also asked to state the chemical or brand names of antibiotics they had used.The survey was self-administrated and was made available online in both Arabic and English via a WhatsApp application.The internal consistency of COVID-19 and antibiotics (part 3 of the questionnaire) was determined by Cronbach's alpha and was 0.729, which indicates very good reliability.

Ethical Considerations
A letter of information explaining the study's objectives, confidentiality, and voluntary participation was sent out with the questionnaire.The continued filling of the questionnaire is considered a consent form.The questionnaire respects the total anonymity of the participants.The Hiram Hospital's scientific and ethical committee gave its approval to the study protocol.

Statistical Analysis
To summarize the data on participant demographics and to provide the prevalence of antibiotic use, a descriptive analysis was carried out.Pretesting was done on the questionnaire.SPSS 21 software was used to examine the data once it was automatically saved online and downloaded in Excel format.Every result was double-checked to find any mistakes or discrepancies.According to the results, participants were classified into 2 groups: presenting with the use of antibiotics during COVID-19 infection or not.A bivariate analysis was performed to identify the variables affecting the use of antibiotics using Student's t-test for continuous variables and χ 2 test for categorical variables.At α < 0.05, statistical significance was established.The odds ratios (ORs) and accompanying 95% confidence intervals (CIs) were estimated using bivariate analysis.With SPSS 21, all statistical analyses were completed.
However, among the responders, 31.4% (n = 150) reported seeing a doctor to address the COVID-19 infection, and 7.7% (n = 37) reported being admitted to the hospital.Moreover, among the subjects, 40.2% (n = 192) were receiving antibiotic medication during the COVID-19 infection.Furthermore, the majority of participants who took antibiotics during their COVID-19 infection took one antibiotic, whereas the remaining participants took two (76.1%,n = 146 and 23.9%, n = 46, respectively); antibiotic treatment was prescribed by several people.A physician's prescription is mentioned by some participants (51%, n = 98), followed by a pharmacist's (23.4%, n = 45), self-taken (14.5%, n = 28), and others as family or friends (10.9%, n = 21).Furthermore, the findings indicated that the primary rationale for using antibiotics was either to lessen symptoms or as a preventative measure (n = 143 for 74.5% and n = 49 for 25.5%, respectively).However, 59.3% (n = 114) of the respondents respected the antibiotic therapy's role, and 40.6% of the respondents (n = 78) discontinued taking the antibiotic when they felt better (Table 2).

Determinants of Antibiotic Misuse
No significant relationship was seen between antibiotic use and gender, BMI, education level, and working in the health field.However, results showed that there was a significant relationship between smoking and severity of symptoms (OR 2.077, 95% CI, 1.336% to 3.229%, p < 0.001) and antibiotic use (OR 1.802, 95% CI, 1.238% to 2.624%, p < 0.002).Similarly, those with COVID-19 infection symptoms that were severe took far more antibiotics (OR 2.318, 95% CI 1.489% to 3.610%, p = 0.000).Furthermore, a nearly significant correlation was seen between the usage of antibiotics and the individuals who were not vaccinated (OR 0.640, 95% CI 0.407% to 1.008%, p = 0.053) (Table 3).Data on the perceived severity of COVID-19 infection (not actual disease severity) and its correlations with gender, smoking status, and hospital admission are displayed in Table 4. Gender and perceived severity were found to be significantly correlated (p-value = 0.046).This shows that men may view their COVID-19 infection as more severe than women do.Additionally, there is a statistically significant correlation between perceived severity and smoking status (p-value = 0.001).Smokers may be more prone to believe that their infection is serious.The largest statistical correlation was found between perceived severity and hospital admission (p-value = 0.000).No significant relationship was seen between nonprescription antibiotic use and gender.Nevertheless, results showed that there was a significant relationship between nonprescription ATB use and education level (p < 0.031) and working in the health sector (p < 0.004).Furthermore, a significant correlation was seen between respecting antibiotic therapy's roles and working in the health sector (p = 0.053) (Table 5).

Discussion
In addition to posing a challenge to global healthcare systems, the COVID-19 pandemic has raised a number of related issues.The misuse of antibiotics is one of the most important of them.Antibiotic resistance is a threat to world health because antibiotics, which are meant to treat bacterial illnesses, are frequently prescribed excessively or overused [18].This issue is made worse by the combination of COVID-19 and antibiotic abuse, posing a dual risk to public health [19].This study aimed to investigate the prevalence of antibiotic misuse during the COVID-19 pandemic in Lebanon.When the participants were asked about the severity of their COVID-19 infection, 28.2% of the cases considered it mild, moderate in 50.2% of the cases, and severe in 21.5% of the cases; 40.2% (n = 192) were receiving antibiotic medication during the COVID-19 infection.Additionally, 76.1% of the participants took one antibiotic during their COVID-19 infection, whereas the remaining participants took two (23.9%).Antibiotic treatment was prescribed by a physician for 51% of the participants, while the rest (49%) used antibiotics without consulting a doctor.Another supply-side player in antibiotic misuse is the pharmacy.It is worth noting that community pharmacists are a main source of healthcare information in the context of limited physician access, and patients frequently seek their services directly.Thus, they could play a significant role in dispensing and recommending antibiotic use to patients.It is imperative that pharmacists possess knowledge about the problem of antibiotic resistance, and policymakers ought to encourage the execution of public education campaigns regarding antibiotic usage in this context [20,21].Moreover, community pharmacists typically have a strong awareness of and negative views regarding selling antibiotics without a prescription.Their procedures do, however, have some noticeable flaws, especially when it comes to patient education about the possible adverse effects of giving antibiotics without a prescription [22].
The majority of antibiotic use worldwide takes place outside of hospitals, and nonprescription antibiotic access is widespread [23,24].In our study, 23.4% took antibiotics after consulting a pharmacist.Concerning the severity of the infection, there was a significant correlation between perceived severity, smoking status, and hospital admission.
The results showed that there was a significant relationship between nonprescription ATB use and education level and working in the health sector.Furthermore, a significant correlation was seen between respect for antibiotic therapy's role and working in the health sector.Antibiotic abuse is more common among those with less education, though this is not always the case.In this study, participants who work in the health sector were more likely to use antibiotics after consulting a doctor, but not all of them respected the prescription rules.When compared to parents, a higher percentage of doctors and pharmacists in a Korean study thought that antibiotics could treat the common cold in children or lessen its complications.This suggests that healthcare professionals may also have false beliefs about the efficacy of antibiotics, similar to the general public [24].A previous review found that more than one-third of patients who were prescribed antibiotics did not appropriately follow through on their antibiotic prescription and that 25% of patients kept any leftover drugs for later use [25].These findings point to a widespread pattern of inadequate antibiotic prescribing and usage practices [26].Another study performed in China found that antibiotic use is significantly influenced by gender, with men less likely than women to keep antibiotics at home or in their dorms.Another significant factor is the parents' educational level, with a university education or higher being linked to a higher chance of keeping antibiotics in the home or dorm.There are variations in antibiotic use according to the province of residency; people from less developed provinces are more likely to misuse antibiotics.A medical background offers protection against some antibiotic usage behaviors [27].
Numerous research studies have revealed that developing countries are experiencing a rise in antibiotic resistance [23].Several strategies may be used to address the issue of antibiotic misuse, such as controlling and monitoring physician prescribing practices to prevent over-prescribing; implementing successful health education programs to teach patients to take antibiotics exactly as prescribed; prohibiting the sale of antibiotics in pharmacies without a prescription; and encouraging patients to dispose of leftover antibiotics.Since this study is cross-sectional, one of its limitations is that it is unable to determine a cause-and-effect link between any variables and the behaviors associated with antibiotic misuse.

Conclusions
The misuse of antibiotics poses a serious threat to world health.Overuse and incorrect use of antibiotics are common problems.Sometimes, despite their ineffectiveness, they are given for viral diseases like the flu and colds.Antibiotic-resistant microorganisms are a result of this usage.Evidently, misusing antibiotics for self-limiting illnesses among participants was high.No significant association was detected between the nonprescription antibiotic use and gender.However, the findings indicated a strong correlation between the usage of nonprescription ATB and employment in the health sector and educational level.Additionally, a strong association was observed between respect for antibiotic therapy's role and employment in the health sector.It is critically necessary to launch a campaign to encourage doctors to prescribe antibiotics appropriately, to enforce laws against the sale of medicines without a prescription, and to inform the public about the treatment of self-limiting illnesses.

Table 1 .
Sociodemographic and other characteristics of participants.

Table 4 .
Association between gender, smoking, and hospital admission with severity of COVID-19 infection.

Table 5 .
Association between nonprescription ATB, respecting ATB therapy's role, and some other characteristics.