• Users Online: 75
  • Print this page
  • Email this page


 
 Table of Contents  
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


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 Submission09-Oct-2022
Date of Acceptance17-Nov-2022
Date of Web Publication31-Dec-2022

Correspondence Address:
Dr. Manea Fares Al Munjem
Department of Pharmaceutical Care, King Khalid Hospital, Ministry of Health, Najran
Saudi Arabia
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/sjcp.sjcp_20_22

Rights and Permissions
  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 Top


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 Top


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 Top


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)

Click here to view
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)

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

Click here to view


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 (%)

Click here to view


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)

Click here to view


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

Click here to view



  Discussion Top


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 Top


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.



 
  References Top

1.
Shapiro DJ, Hicks LA, Pavia AT, Hersh AL Antibiotic prescribing for adults in ambulatory care in the USA, 2007-09. J Antimicrob Chemother 2014;69:234-40.  Back to cited text no. 1
    
2.
Stover CS, Litwin CM The epidemiology of upper respiratory infections at a tertiary care center: Prevalence, seasonality, and clinical symptoms. J Respir Med 2014;2014:469393.  Back to cited text no. 2
    
3.
Doan Q, Enarson P, Kissoon N, Klassen TP, Johnson DW. Rapid viral diagnosis for acute febrile respiratory illness in children in the emergency department. Cochrane Database Syst Rev 2014;9:CD006452.  Back to cited text no. 3
    
4.
Shehab N, Patel PR, Srinivasan A, Budnitz DS Emergency department visits for antibiotic-associated adverse events. Clin Infect Dis 2008;47:735-43.  Back to cited text no. 4
    
5.
Thabit AK, Turkistani SA, Alsubaie SA, Takroni EA, Basaeed LF, Saadawi DW When antibiotics experts say no to antibiotics. Germs 2020;10:380-4.  Back to cited text no. 5
    
6.
Williams A, Mathai AS, Phillips AS Antibiotic prescription patterns at admission into a tertiary level intensive care unit in northern India. J Pharm Bioallied Sci 2011;3:531-6.  Back to cited text no. 6
    
7.
Woolhouse M, Waugh C, Perry MR, Nair H Global disease burden due to antibiotic resistance: State of the evidence. J Glob Health 2016;6:010306.  Back to cited text no. 7
    
8.
Thabit AK, Crandon JL, Nicolau DP Antimicrobial resistance: Impact on clinical and economic outcomes and the need for new antimicrobials. Expert Opin Pharmacother 2015;16:159-77.  Back to cited text no. 8
    
9.
Barlam TF, Cosgrove SE, Abbo LM, MacDougall C, Schuetz AN, Septimus EJ, et al. Implementing an antibiotic stewardship program: Guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin Infect Dis 2016;62:e51-77.  Back to cited text no. 9
    
10.
van der Velden AW, Pijpers EJ, Kuyvenhoven MM, Tonkin-Crine SK, Little P, Verheij TJ Effectiveness of physician-targeted interventions to improve antibiotic use for respiratory tract infections. Br J Gen Pract 2012;62:e801-7.  Back to cited text no. 10
    
11.
Ong DS, Kuyvenhoven MM, van Dijk L, Verheij TJ Antibiotics for respiratory, ear and urinary tract disorders and consistency among GPs. J Antimicrob Chemother 2008;62:587-92.  Back to cited text no. 11
    
12.
Redmond NM, Turnbull S, Stuart B, Thornton HV, Christensen H, Blair PS, et al. Impact of antibiotics for children presenting to general practice with cough on adverse outcomes: Secondary analysis from a multicentre prospective cohort study. Br J Gen Pract 2018;68:e682-93.  Back to cited text no. 12
    
13.
Stelter K Tonsillitis and sore throat in children. GMS Curr Top Otorhinolaryngol Head Neck Surg 2014;13:Doc07.  Back to cited text no. 13
    
14.
Meyer KC Lung infections and aging. Ageing Res Rev 2004;3:55-67.  Back to cited text no. 14
    
15.
Mahashur A Management of lower respiratory tract infection in outpatient settings: Focus on clarithromycin. Lung India 2018;35:143-9.  Back to cited text no. 15
    
16.
Ozdemir S, Ozturk TC, Metiner Y, Ak R, Ocal O Evaluation of the prescriptions written for upper respiratory tract infections. North Clin Istanb 2015;2:107-14.  Back to cited text no. 16
    
17.
Shulman ST, Bisno AL, Clegg HW, Gerber MA, Kaplan EL, Lee G, et al; Infectious Diseases Society of America. Clinical practice guideline for the diagnosis and management of group A streptococcal pharyngitis: 2012 update by the Infectious Diseases Society of America. Clin Infect Dis 2012;55: e86-102.  Back to cited text no. 17
    
18.
Shin SM, Shin JY, Kim MH, Lee SH, Choi S, Park BJ Prevalence of antibiotic use for pediatric acute upper respiratory tract infections in Korea. J Korean Med Sci 2015;30:617-24.  Back to cited text no. 18
    
19.
Hagedoorn NN, Borensztajn DM, Nijman R, Balode A, von Both U, Carrol ED, et al; PERFORM consortium. Variation in antibiotic prescription rates in febrile children presenting to emergency departments across Europe (MOFICHE): A multicentre observational study. PLoS Med 2020;17:e1003208.  Back to cited text no. 19
    
20.
Olwi RI, Olwi DI Trends in the use of antibiotics for pharyngitis in Saudi Arabia. J Infect Dev Ctries 2021;15:415-21.  Back to cited text no. 20
    
21.
Haseeb A, Faidah HS, Algethamy M, Alghamdi S, Alhazmi GA, Alshomrani AO, et al. Antimicrobial usage and resistance in Makkah region hospitals: A regional point prevalence survey of public hospitals. Int J Environ Res Public Health 2021;19:254.  Back to cited text no. 21
    
22.
Albuhairi S, Farhan MA, Alanazi S, Althaqib A, Albeladi K, Alarfaj S, et al. Antibiotic prescribing patterns for hospitalized children with community-acquired pneumonia in a secondary care center. J Infect Public Health 2021;14:1035-41.  Back to cited text no. 22
    
23.
Metlay JP, Waterer GW, Long AC, Anzueto A, Brozek J, Crothers K, et al. Diagnosis and treatment of adults with community-acquired pneumonia. An official clinical practice guideline of the American Thoracic Society and Infectious Diseases Society of America. Am J Respir Crit Care Med 2019;200:e45-67.  Back to cited text no. 23
    
24.
Kalil AC, Metersky ML, Klompas M, Muscedere J, Sweeney DA, Palmer LB, et al. Executive summary: Management of adults with hospital-acquired and ventilator-associated pneumonia: 2016 clinical practice guidelines by the Infectious Diseases Society of America and the American Thoracic Society. Clin Infect Dis 2016;63:575-82.  Back to cited text no. 24
    
25.
Alradini F, Bepari A, AlNasser BH, AlGheshem EF, AlGhamdi WK Perceptions of primary health care physicians about the prescription of antibiotics in Saudi Arabia: Based on the model of theory of planned behaviour. Saudi Pharm J 2021;29:1416-25.  Back to cited text no. 25
    
26.
Harakeh S, Almatrafi M, Ungapen H, Hammad R, Olayan F, Hakim R, et al. Perceptions of medical students towards antibiotic prescribing for upper respiratory tract infections in Saudi Arabia. BMJ Open Respir Res 2015;2:e000078.  Back to cited text no. 26
    
27.
Cormican MG, Jones RN Susceptibility to levofloxacin predicted from in vitro susceptibility testing results obtained with ciprofloxacin and with ofloxacin. J Clin Microbiol 1995;33:215-6.  Back to cited text no. 27
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Materials and Me...
Results
Discussion
Conclusion
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed610    
    Printed26    
    Emailed0    
    PDF Downloaded37    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]