Prescription patterns and antibiotic resistance rates of respiratory tract infections in a Saudi tertiary medical centre

Manea Fares Al Munjem; Abrar K Thabit; Sahibzada Tasleem Rasool; Promise Madu Emeka; Fahad Fares Al Munajjim; Mohd Al Habeeb

doi:10.4103/sjcp.sjcp_20_22

ORIGINAL ARTICLE

Year : 2022 | Volume : 1 | Issue : 4 | Page : 128-133

Prescription patterns and antibiotic resistance rates of respiratory tract infections in a Saudi tertiary medical centre

Manea Fares Al Munjem¹, Abrar K Thabit², Sahibzada Tasleem Rasool³, Promise Madu Emeka³, Fahad Fares Al Munajjim⁴, Mohd Al Habeeb⁵
¹ Department of Pharmaceutical Care, King Khalid Hospital, Ministry of Health, Najran (formerly John Hopkins Aramco Health Care, Dhahran, Saudi Arabia), Saudi Arabia
² Department of Pharmacy Practice, Faculty of Pharmacy, King Abdulaziz University, Jeddah, Saudi Arabia
³ Department of Biomedical Sciences, Collage of Clinical Pharmacy, King Faisal University, Hafuf, Saudi Arabia
⁴ College of Medicine, Najran University, Najran, Saudi Arabia
⁵ Department of Pharmaceutical Care, John Hopkins Aramco Health Care, Dhahran, Saudi Arabia

Date of Submission	09-Oct-2022
Date of Acceptance	17-Nov-2022
Date of Web Publication	31-Dec-2022

Correspondence Address:
Dr. Manea Fares Al Munjem
Department of Pharmaceutical Care, King Khalid Hospital, Ministry of Health, Najran
Saudi Arabia

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/sjcp.sjcp_20_22

Abstract

Objectives: Respiratory tract infections (RTIs) are a significant cause of hospitalization due to morbidity and mortality. The unwise use of antimicrobial agents in RTI management may contribute to the emergence of bacterial resistance. Therefore, we aimed to assess prescription patterns and antibiotic resistance among hospitalized patients with RTIs. Materials and Methods: This retrospective study included patients with any RTI who were hospitalized between 2016 and 2017. Antibiotics prescribed and changes in antibiotic resistance over time were evaluated. Results: The 405 included patients ranged in age from a few months old to over 65 years old. The most common clinical manifestations were fever (98% of patients) and sore throat (57.5%), followed by cough (46.7%) and dyspnea (27.2%). C-reactive protein was elevated in 43%. The most common diagnoses among all the patients were tonsillitis (43.2%), pharyngitis (36%), and pneumonia (23%). The most commonly isolated organisms were Haemophilus influenza (93.2%), Streptococcus pneumoniae (90.9%), Pseudomonas aeruginosa (84.1%), and Klebsiella pneumoniae (84.1%). Amoxicillin/clavulanate was mostly prescribed for upper RTIs, whereas levofloxacin was mostly prescribed for lower RTIs. Amoxicillin/clavulanate was the major antibiotic prescribed for pediatric patients, whereas geriatric patients (≥65 years) were mostly prescribed levofloxacin. No major changes in resistance rates were observed for amoxicillin/clavulanate, levofloxacin, or ciprofloxacin before (in 2015), during the study period (2016–2017), and after the study (2018). Conclusion: Amoxicillin/clavulanate and levofloxacin were the most commonly prescribed antibiotics, but resistance to these antibiotics did not increase over time. However, clinicians should make every attempt to collect cultures from patients with severe RTIs to rule out bacterial involvement.

Keywords: Amoxicillin/clavulanate, antibiotic, levofloxacin, resistance, respiratory culture, respiratory tract infection, pneumonia, URTI

How to cite this article:
Al Munjem MF, Thabit AK, Rasool ST, Emeka PM, Al Munajjim FF, Al Habeeb M. Prescription patterns and antibiotic resistance rates of respiratory tract infections in a Saudi tertiary medical centre. Saudi J Clin Pharm 2022;1:128-33

How to cite this URL:
Al Munjem MF, Thabit AK, Rasool ST, Emeka PM, Al Munajjim FF, Al Habeeb M. Prescription patterns and antibiotic resistance rates of respiratory tract infections in a Saudi tertiary medical centre. Saudi J Clin Pharm [serial online] 2022 [cited 2023 Feb 2];1:128-33. Available from: http://www.sjcp.org/text.asp?2022/1/4/128/366503

Introduction

Respiratory tract infections (RTIs) are very common, and hence considered the most common reason for antibiotic prescriptions.^[1] Most upper respiratory infections are caused by viruses, but viral infections can also result in pneumonia, as can occur with influenza and coronavirus disease-2019. Conversely, bacterial RTIs can involve the pharynx, epiglottis, and lungs. An association between respiratory viral/bacterial infections has been documented and can be predicted.^[2]

The use of antibiotics in viral infections has not been reduced by routine rapid viral testing, which is only available to detect some, but not all, respiratory viruses.^[3] Hence, unnecessary use of antibiotics ensues, leading to the rise and spread of antibiotic-resistant bacteria, as well as increases in emergency department visits due to antibiotic-related adverse effects.^[4],[5] Multiple broad-spectrum antibiotics are also commonly prescribed to patients admitted with RTIs.^[6] This rise in antibiotic prescriptions can also increase avoidable treatment costs and antibiotic expenditures.^[7] Worldwide misuse of antibiotics is one of the major reasons that are triggering a global emergence and spread of new resistance mechanisms, making the treatment of common infectious diseases more difficult and resulting in lengthy hospital stays, disability, and loss of life.^[8],[9]

In Saudi Arabia, the currently available data are insufficient to establish associations between the pattern of antibiotic prescriptions and antibiotic resistance rates, especially in the setting of RTIs. Therefore, the aim of this study was to investigate the antibiotic prescribing patterns in patients with RTIs and antibiotic resistance observed in a tertiary hospital in Saudi Arabia.

Materials and Methods

Study design and patients

This retrospective cohort study was conducted at a 380-bed tertiary care hospital with five intensive care units. Hospitalized patients of all ages, including pediatrics (0–17 years) and adults (≥18 years) who had an upper or lower RTI and who were prescribed antibiotic therapy between January 2016 and December 2017, were included in the study. The study protocol was approved by the institutional review board (reference No. 18-15, dated November 24, 2016), which waived the requirement for informed consent given the retrospective nature of the study. Confidentiality of the data was maintained as each patient was coded and the data were stored in a locked computer.

Data collection and analysis

Study data were collected from the patients’ electronic medical records, which included basic demographics, past medical history, antibiotics used within 90 days before hospital admission, RTI diagnosis (from the progress notes), respiratory bacterial culture and susceptibility results, and prescribed antibiotics. Antimicrobial susceptibility trends from 2015 to 2017 were collected from the general hospital antibiograms to identify any potential changes over time. The results were presented using descriptive statistics, as numbers and percentages, using the Statistical Package for the Social Sciences (SPSS) software program, version 24.0 (SPSS, Chicago, Illinois).

Results

A total of 405 patients met the eligibility criteria. The basic demographics of the included patients, the clinical characteristics of their RTIs, and the prescribed antibiotics are listed in [Table 1]. Patients aged less than 20 years represented a significant population of patients with lower and upper RTIs. The most common chief complaint was fever (98.5%), followed by sore throat (57.5%), cough (46.7%), and dyspnea (27.2%). All patients had leukocytosis. The most prevalent lower RTI was pneumonia (23% of all patients; 47.4% of all patients with lower RTI, n = 196), whereas tonsillitis and pharyngitis were the most common upper RTI (43.2% and 36% of all patients; 50% and 41.7% of all patients with upper RTI, n = 350). [Figure 1] shows the distribution of RTIs among the different age groups. [Table 2] lists the antibiotics that were used by some patients within 90 days before hospital admission, where amoxicillin/clavulanate and levofloxacin were used by 45.7% and 36.5%, respectively.

Table 1: Basic demographics and clinical characteristics of patients (n = 405)

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Figure 1: Percentage of patients with (A) lower respiratory tract infections and (B) upper respiratory tract infections, according to their age group (P < 0.0001 for all comparisons)

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Table 2: Antibiotics used for respiratory infections within 90 days before hospital admission (n = 405)

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Respiratory culture and susceptibility reports were available from 44 (10.9%) patients from whom a respiratory specimen was collected and sent to the microbiology lab. Most of these patients had pneumonia (n = 41; 92%). Most cultures (n = 41; 92%) were polymicrobial, where the most frequently isolated organisms (from either polymicrobial or monomicrobial cultures) were Haemophilus influenza (93.2%), Streptococcus pneumoniae (93%), Klebsiella pneumoniae (86%), and Pseudomonas aeruginosa (86%). These were followed by monomicrobial cultures of S. pneumoniae (n = 2; 0.5%) and H. influenzae (n = 1; 0.2%). Staphylococcus aureus was isolated from only 23.3% of all positive cultures. Susceptibilities of isolated bacteria are shown in [Table 3].

Table 3: Susceptibilities of isolated bacteria to different antibiotics, n (%)

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The antibiotic prescribing pattern for the different RTIs is illustrated in [Figure 2]. Amoxicillin/clavulanate was mostly prescribed for upper RTIs and in pediatrics, whereas levofloxacin was mostly prescribed for lower RTIs and in geriatrics (≥65 years). Azithromycin was mainly prescribed for bronchitis (53.3%) as shown in [Figure 2].

Figure 2: Antibiotic prescribing pattern for (A) lower respiratory tract infections and (B) upper respiratory tract infections (P < 0.0001 for all comparisons)

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The antibiotic susceptibility trends over the course of 4 years (2015–2018) for the reported antibiotics, as derived from the hospital’s antibiograms, are depicted in [Figure 3]. No changes were observed in the susceptibility of K. pneumoniae and S. aureus to the tested antibiotics. The susceptibility of S. pneumoniae to levofloxacin remained at 100% throughout the study period. Of note, our hospital antibiograms lack data for susceptibility to azithromycin.

Figure 3: Susceptibility trends of certain respiratory antibiotics against (A) Klebsiella pneumoniae and (B) Staphylococcus aureus

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Discussion

RTIs are the most common causes of hospital and clinic visits among children and adults, and viruses cause the majority of these cases.^[10] However, antibiotics are frequently prescribed for tonsillitis, pharyngitis, sinusitis, and bronchitis, as bacteria can be implicated in these infections.^[11] In this study, we examined the antibiotic prescribing patterns for RTIs and the trends of resistance over the course of the 4-year study. The significant proportion of pediatric patients in our study was consistent with previous reports, as this is the age group mostly hospitalized due to RTIs.^[12] Tonsillitis, accompanied by fever, sore throat, and cough, was reported in 89.2% of patients in the age group of 0–19 years, in agreement with the findings of Stelter.^[13] In contrast, adult patients were mostly hospitalized due to pneumonia (90/226 or 39.8% of patients aged >19 years) or pharyngitis (138/226 or 61.1% of patients aged >19 years), in accordance with the findings reported by Meyer,^[14] who showed that aging represents a risk factor for pneumonia. The annual incidence of pneumonia is estimated at 24.8 in 10,000 patients aged ≥65 years.^[15] Overall, tonsillitis and pharyngitis were the most common upper RTIs in our study, accounting for 50% and 41.7% of the reported infections, respectively. A similarly high occurrence of these two infections was also reported by Ozdemir et al.,^[16] where pharyngitis was seen in 71.4% of the patients and tonsillitis in 22.1%. Notably, as shown in [Figure 2] many of the patients who were diagnosed with tonsilitis or pharyngitis were prescribed amoxicillin/clavulanate (85.1% and 7.5%, respectively) when penicillin or amoxicillin alone would have been sufficient. This is because the causative organism of these infections is S. pyogenes, which does not produce penicillinase warranting the addition of clavulanate.^[17] As a result, the use of amoxicillin/clavulanate instead of amoxicillin alone may contribute to increasing resistance pressure, more diarrhea, and unnecessary costs.

Antibiotics are widely prescribed for RTIs, despite the recognition of their limited benefit in viral infections.^[18] Diagnostic uncertainty is the main driver for antibiotic prescribing.^[19] In Saudi Arabia, current estimates indicate that approximately 40% of RTI cases are treated with antibiotics.^[20] One study from Makkah, Saudi Arabia, reported pneumonia as the top indication for antimicrobial prescribing, accounting for 17.3% of 710 hospitalized patients.^[21] In our study, amoxicillin/clavulanate was usually prescribed for both upper and lower RTIs for all patients aged 0–35 years, in concurrence with a previously reported pattern.^[16] Amoxicillin/clavulanic was the most frequently prescribed agent for children, consistent with a recently published report in which 57.9% of 233 pediatric patients received it for community-acquired pneumonia.^[22] In general, the use of levofloxacin for the treatment of lower RTIs in this study complied with the guidelines of the Infectious Diseases Society of America for the treatment of community and hospital-acquired pneumonia, as fluoroquinolones are indicated as first-line agents.^[23],[24] Nonetheless, levofloxacin is typically not preferred to be widely used in Saudi Arabia due its activity in tuberculosis, which is endemic in the country, and its use may result in increased rates of mycobacterial resistance to fluoroquinolones.

Antibiotic misuse can result in the emergence of antibiotic resistance, as well as the development of superinfections, prolonged hospitalizations, and unnecessary increases in healthcare costs.^[8] One study assessing the perceptions of Saudi primary care physicians toward antibiotic prescribing and knowledge of antibiotic resistance found a trend suggesting an association between overprescribing of antibiotics and poor knowledge of antibiotic resistance.^[25] Another study that investigated the perceptions of 1,042 Saudi medical students regarding antibiotic prescribing for upper RTIs reported that almost all the students (97.2%) had self-medicated themselves with antibiotics during the previous year, with the majority reported antibiotic use for upper RTI symptoms (61.8%).^[26] Notably, some respondents (18.1%) assumed that antibiotics are also effective against viral infections. Fortunately, knowledge about appropriateness of antibiotics for bacterial infections only improved as students progress to advanced years of college as senior students provided more correct responses to the questions that evaluated this knowledge compared with their junior counterparts. Given the results of these studies and the negative impact of antibiotic resistance on clinical and economic outcomes, antibiotic prescribers and medical trainees should be better educated on the appropriate prescribing of antibiotics and how to differentiate between bacterial infections and conditions that may resemble them, such as viral infections or malignancy.^[5],[18] Continuing medical education can be an effective venue for conveying information on appropriate antibiotic-prescribing behavior, as recommended by Alradini et al.^[25]

Antimicrobial stewardship policies and protocols should also be implemented to enforce prudent antibiotic utilization.^[9] One important measure for tracking the appropriate use of antibiotics within an institution is to review the changes occurring in antibiotic susceptibility in the annual antibiogram from year to year and to make note of antibiotics that require attention and potential interventions, such as observation or restriction. Based on our institution’s annual antibiograms, the susceptibility trends for K. pneumoniae and S. aureus to amoxicillin/clavulanate and ciprofloxacin did not change over the four consecutive years of our study, with no elevation in the resistance rate. Data on susceptibility of K. pneumoniae to levofloxacin were not reported as ciprofloxacin susceptibility can be used as a surrogate.^[27]

This study has some limitations. First, it was conducted in a single center; hence, our conclusions may not be generalizable to other institutions or populations. Second, data on type of respiratory specimens and antibiotics utilization over the years to correlate with resistance data from the antibiograms were not collected and assessed to give a better picture on the impact of antibiotic use on the resistance trend. Third, we did not evaluate the readmission rates, with costs, to include recommendations regarding these outcomes. Finally, our institution does not routinely screen for viral RTIs to exclude unnecessary antibiotic use.

Conclusion

Our study showed that our institution follows good practices when administering antibiotics. Although amoxicillin/clavulanate and levofloxacin were the most commonly prescribed antibiotics, resistance to these antibiotics did not increase over the course of the 4-year study period. However, clinicians should make every attempt to collect cultures from patients with severe RTIs to rule out bacterial involvement. Further studies on different infections are recommended to determine the overall impact of antibiotic prescribing on antibiotic resistance.

Ethical policy and institutional review board statement

The study design was approved by the institutional review board of Johns Hopkins Healthcare (Reference No. 18-15, dated November 24, 2016).

Financial support and sponsorship

Not applicable.

Conflicts of interest

There are no conflicts of interest.

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