Next Article in Journal
Lung Ultrasound B-lines Occurrence in Relation to Left Ventricular Function and Hydration Status in Hemodialysis Patients
Previous Article in Journal
The Effects of High-Intensity Interval Exercise and Hypoxia on Cognition in Sedentary Young Adults
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Medicina
Volume 55
Issue 2
10.3390/medicina55020044
medicina-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Antibiotic Prescribing Practices and Errors among Hospitalized Pediatric Patients Suffering from Acute Respiratory Tract Infections: A Multicenter, Cross-Sectional Study in Pakistan

by
Sadia Iftikhar
1,
Muhammad Rehan Sarwar
1,2,*,
Anum Saqib
2,
Muhammad Sarfraz
2,3 and
Qurat-ul-ain Shoaib
4
1
Akhtar Saeed College of Pharmaceutical Sciences, Lahore 54000, Pakistan
2
Department of Pharmacy, The Islamia University of Bahawalpur, Bahawalpur 63100, Punjab, Pakistan
3
College of Pharmacy, Al Ain University of Science and Technology, Al Ain, PO Box 64141, Abu Dhabi, UAE
4
College of Pharmacy, University of the Punjab, Lahore 54000, Pakistan
*
Author to whom correspondence should be addressed.
Medicina 2019, 55(2), 44; https://doi.org/10.3390/medicina55020044
Submission received: 5 October 2018 / Revised: 29 January 2019 / Accepted: 5 February 2019 / Published: 11 February 2019
Versions Notes

Abstract

:
Background and objective: The noncompliance of treatment guidelines by healthcare professionals, along with physiological variations, makes the pediatric population more prone to antibiotic prescribing errors. The present study aims to evaluate the prescribing practices and errors of the most frequently prescribed antibiotics among pediatric patients suffering from acute respiratory tract infections who had different lengths of stay (LOS) in public hospitals. Methods: A retrospective, cross-sectional study was conducted in five tertiary-care public hospitals of Lahore, Pakistan, between 1 January 2017 and 30 June 2017. The study population consisted of pediatric inpatients aged 0 to 9 years. Results: Among the 11,892 pediatric inpatients, 82.8% were suffering from lower acute respiratory tract infections and had long LOS (53.1%) in hospital. Penicillins (52.4%), cephalosporins (16.8%), and macrolides (8.9%) were the most frequently prescribed antibiotics. Overall, 40.8% of the cases had antibiotic prescribing errors related to wrong dose (19.9%), wrong frequency (18.9%), and duplicate therapy (18.1%). Most of these errors were found in the records of patients who had long LOS in hospital (53.1%). Logistic regression analysis revealed that the odds of prescribing errors were lower in female patients (OR = 0.6, 95% CI = 0.1–0.9, p-value = 0.012). Patients who were prescribed with ≥3 antibiotics per prescription (OR = 1.724, 95% CI = 1.1–2.1, p-value = 0.020), had long LOS (OR = 12.5, 95% CI = 10.1–17.6, p-value < 0.001), and were suffering from upper respiratory tract infections (URTI) (OR = 2.8, 95% CI = 1.7–3.9, p-value < 0.001) were more likely to experience prescribing errors. Conclusion: Antibiotics were commonly prescribed to patients who had long LOS. Prescribing errors (wrong dose, wrong frequency, and duplicate therapy) were commonly found in cases of lower respiratory tract infections (LRTIs), especially among those who had prolonged stay in hospital.

1. Introduction

Acute respiratory tract infections (ARTIs), i.e., upper respiratory tract infections (URTIs) and lower respiratory tract infections (LRTIs), are responsible for increased morbidity and mortality rates among children [1,2]. Children are more prone to ARTIs because of their weak immune system and constant contact with persons who could be carriers [3]. According to an estimation made by the World Health Organization (WHO), ARTIs account for 20% of all the childhood deaths [4]. Globally, 40% of the mortalities due to ARTIs have been reported in developing countries like Nepal, Bangladesh, Indonesia, and India [5]. According to an estimate made by the World Bank collection of development indicators, the prevalence of ARTIs among Pakistani children was found to be 17.7% in 2013. However, only 60.3% of them could get access to treatment [6].
Most of the ARTIs are caused by viruses, but the unnecessary prescribing of antibiotics like penicillins, cephalosporins, and macrolides in children suffering from ARTIs is a common practice globally [7]. In many healthcare settings, the antibiotic prescribing rate is twice as much as the expected rate of antimicrobial needed [8]. Although various international guidelines recommend the limited use of antibiotics in ARTIs, the noncompliance of these guidelines and the frequency of prescribing antibiotics in these infections is common in the healthcare system of Pakistan [9,10]. Evidence suggests that the unwanted use of antibiotics (e.g., cephalosporins) in pneumonia and bronchitis has economically burdened the healthcare system by causing a significant increase in the incidence of antimicrobial resistance, prescribing errors, and patients’ length of stay (LOS) in hospital [11,12].
The term “prescribing errors” can be defined as “the prescribing decision that cause an unintentional and significant reduction in the effectiveness of the treatment or increase in the risk of harm compared to the with the practices mentioned in standard treatment guidelines” [13]. The Infectious Diseases Society of Pakistan (IDSP) guidelines for antibiotic use are available in Pakistan [14], but the nonadherence to national and international guidelines and the unavailability of national formularies for the pediatric population could be possible causes of these errors [15]. The incidence of prescribing errors is common in pediatric patients due to age, weight-based dose adjustment, interpatient variability, need of dilution for stock medicines, and altered pharmacokinetic properties of drugs [16]. A study revealed 3–20% errors in prescriptions in the pediatrics inpatient ward [17]. In Pakistan, data of mortality and hospital admissions due to medication prescribing errors is not officially recorded. However, the Pakistan Society of Health System Pharmacists (PSHP) has roughly estimated deaths of 400,000 to 500,000 people (including women and children) annually due to medication errors [18]. Among all the errors, dosing errors are more common in prescription of pediatric patients [19]. Getting an insight about antibiotic prescribing practices and the associated errors among the pediatric population is crucial to improve the current policies and to prevent this population from untoward effects. Therefore, the objective of this study is to compare the antibiotic prescribing pattern and to identify common medication errors in the treatment of ARTIs among pediatric patients with short and long LOS in hospital.

2. Methods

2.1. Study Design and Settings

A retrospective, cross-sectional study was conducted in five public hospitals (Mayo Hospital, Jinnah Hospital, General Hospital, Services Hospital, and Children’s Hospital) of Lahore, Pakistan. Data were collected between 1 January 2017 and 30 June 2017. The selected hospitals were tertiary-care hospitals providing healthcare services to children in the pediatric department. The characteristics of the selected hospitals are summarized in Supplementary S1.

2.2. Study Population and Sample Size

According to hospital records, a total of 249,653 patients (age = 0−9 years) visited the outpatient departments (OPDs) and 86,227 (age = 0−9 year) were admitted during the six-month study period. Among the inpatients, 13,582 were diagnosed with ARTIs. The medical records of all patients aged >9 years were excluded. Participants were included in the study if they were suffering from one ARTI, prescribed with antibiotics after diagnosis of ARTIs, and had no previous medical history of RTIs. The records of 1730 participants who did not meet the inclusion criteria were excluded from the study. Consequently, records of 11,852 inpatients were finally selected for the study (Supplementary S2).

2.3. Data Collection

A data collection form was developed consisting of four main parts: (1) characteristics of the patients, (2) diagnosis, (3) recommended antibiotics, and (4) prescribing errors (Supplementary S3). The 2nd edition of the International Classification of Primary Care (ICPC-2) was used to define ARTIs as a clinical diagnosis of LRTIs, acute bronchitis (R 78), pneumonia (R 81), and epiglottitis (R 83). The URTIs included tonsillitis (R 76), whooping cough (R 71), acute bacterial sinusitis (R 75), laryngitis and tracheitis (R 77), and other URTIs, including common cold (R 74) [20]. The Anatomical Therapeutic Chemical (ATC) classification system [21] was used for the coding of antibiotics. The data relating to dose, dosage form, frequency, and duration of prescribed antibiotics were extracted by reviewing patient records according to the criteria (Supplementary S4). Appropriateness of prescribing antibiotics was assessed by critically observing and evaluating each of following indicators: drug selection, dosage form, frequency, prescribed quantity, and duration of therapy (Supplementary S4). The assessment of antibiotic prescribing errors was made by taking into account the clinical judgments, nature and severity of underlying disease, and social factors that may contribute to lengthening the patient’s stay time in hospital. Four investigators were assigned to each selected setting; the principal investigator trained all investigators prior to the survey for the collection and validation of data. During the survey, two investigators filled out the investigational form, and the other two reviewed the medical records of patients. The LOS was evaluated by measuring the difference between the date of admission and the date of discharge [22].

2.4. Variables

All the prescribing errors were considered as a dependent variable. The following characteristics were the independent variables and evaluated in the data: gender (1 = male and 0 = female); age (1 = newborn to toddler, 0–3 years; 0 = otherwise), LOS (1 = short, <5 days; 0 = long, ≥5 days); acute respiratory tract infections (1 = LRTI; 0 = URTI).

2.5. Definitions

  • Prescription errors: Incorrect or inappropriate drug selection (based upon indications, contraindications, and other factors), dose, route, rate of administration, frequency, or duplication of drugs.
  • Wrong frequency: Drugs prescribed in a frequency other than that recommended by the guidelines.
  • Wrong dose: Prescribed dose greater than or less than 10% of the recommended dose in the guidelines.
  • Wrong route: Prescribed drug administered by a route other than the recommended route mentioned in the guidelines.
  • Wrong duration: Drugs prescribed for a duration other than that recommended in the guidelines.
  • Duplicate therapy: Two or more drugs prescribed from the same class.

2.6. Data Analysis

Descriptive statistics were used to present the data. Furthermore, logistic regression analysis was performed to figure out the factors associated with prescribing errors. Results were expressed as odds ratio (OR) accompanied by 95% confidence intervals (95% CI), and a p-value < 0.05 was used for statistical significance of differences. Statistical Package for Social Sciences (IBM Corp. Released 2012. IBM SPSS Statistics for Windows Version 21.0. Armonk, NY: IBM Corp.) and Microsoft Excel (MS Office 2010) were used for data analysis.

2.7. Ethics Approval

The ethical approval was obtained from the Pharmacy Research Ethics Committee (PREC) at Akhtar Saeed College of Pharmaceutical Sciences (Reference: 19-2016/PREC, 26 December 2016). Before conducting the study, permission was obtained from hospital administrators.

3. Results

3.1. Characteristics of the Patients

Overall, 40.3% (4781) of the patients were aged 0–3 years, and 43.9% (n = 5202) were 3–10 kg in weight. Of the participants, 50.9% (n = 6033) were prescribed with two antibiotics per prescription, and 53% (n = 6285) of patients were admitted for >5 days, i.e., long LOS (Table 1).

3.2. Antibiotic Prescribing Practices

As the present study was conducted in multiple settings, different international guidelines were found to be implemented for different purposes. It was observed that the Current Medical Diagnosis and Treatment (CMDT) [23] and WHO guidelines were used for diagnosis, while the British National Formulary (BNF) [24] was consulted for doses. The American Academy of Family Physicians (AAFP), the American Academy of Pediatrics, the National Institute of Health and Clinical Excellence (NICE) guidelines on RTIs [25], and the American Thoracic Society Consensus Guidelines were consulted for treatment of pneumonia [26]. The IDSP guidelines [27] were considered for assessing the rational use of antibiotics.
A total of 26,883 antibiotics were prescribed to 11,852 patients. Out of this, 86.9% (n = 23,383) of the antibiotics were prescribed to patients suffering from LRTIs, while 13.1% (n = 3500) were prescribed to patients with URTIs. The practice of prescribing antibiotics was found to be more frequent among patients who had long LOS (52.9%, n = 14,217) compared to those who had short LOS (47.1%, n = 12,666). Most of the children were hospitalized due to LRTIs, especially pneumonia (short LOS = 72.9%, long LOS = 90.8%) (Supplementary S5 and S6). Amoxicillin (short LOS = 82.7%, long LOS = 82.8%) and ampicillin (short LOS = 61.8%, long LOS = 61.7%) were the most commonly prescribed antibiotics in pneumonia. Tonsillitis and pharyngitis were the most commonly observed URTIs among inpatients, and azithromycin (short LOS = 31%, long LOS = 47.9%) and amoxicillin (short LOS = 48.1%, long LOS = 30.8%) were the most frequently prescribed antibiotics for this condition (Supplementary S5 and S6).
In ARTIs, antibiotics were more frequently prescribed to patients who had long LOS in hospital compared to those who had short LOS. Penicillins (52.4%, n = 14,096), cephalosporins (16.8%, n = 4506), and macrolides (8.9%, n = 2404) were among the most commonly prescribed classes of antibiotics (Supplementary S7). Amoxicillin, ampicillin, ceftriaxone, and azithromycin were commonly prescribed antibiotics to patients who had long LOS compared to those who had short LOS in the healthcare settings (Table 2).

3.3. Antibiotic Prescribing Errors

A total of 4836 (40.8%) records had prescribing errors. Most of the errors were found among patients with LRTIs (82.8%) compared to URTIs (17.2%). 47.2% cases had one error, 21.7% had two errors, while more than three errors were found in 30.9% of those cases in which errors were identified. Wrong dose (especially underdosing), wrong frequency (especially high frequency), and duplicate therapy were the most common errors (Table 3). A large number of errors were found in the records of patients who were hospitalized for long periods of time (45.8%) compared to those who had short LOS (35.2%) (Supplementary S8).

3.4. Determinants Associated with Prescribing Errors among Pediatrics Patients

Logistic regression analysis revealed that the odds of prescribing errors decreased by 33% in female patients (OR = 0.6, 95% CI = 0.1–0.9, p-value = 0.012) compared to male patients. The odds of prescribing errors were 1.7 times higher in patients who were prescribed with ≥3 antibiotics per prescription (OR = 1.7, 95% CI = 1.1–2.1, p-value = 0.020) compared to those who were prescribed with one antibiotic per prescription. In patients with long LOS, the odds of prescribing errors were 12.5 times higher (OR = 12.5, 95% CI = 10.1–17.6, p-value < 0.001) compared to patients who had short LOS, while the odds of prescribing errors in patients suffering from URTIs were 2.8 times higher (OR = 2.8, 95% CI = 1.7–3.9, p-value < 0.001) compared to those who were suffering from LRTIs (Table 4).

4. Discussion

The present study set out to determine the antibiotic prescribing practices among the pediatric population suffering from ARTIs and the medication errors in the prescription records of inpatients with different LOS in hospital.

4.1. Antibiotic Prescribing Practices among Pediatric Patients

Our findings revealed that most of the patients suffering from LRTIs were prescribed with penicillins, while macrolides and cephalosporins were prescribed for URTIs. Among these, amoxicillin, ampicillin, and gentamicin were more frequently prescribed to patients who had long LOS compared to those who had short LOS in the healthcare settings. Evidence from previously published studies suggests that a majority of pediatric patients living in Pakistan are prescribed with cephalosporins after every five hours [28,29]. The unnecessary antibiotic prescribing practices in childhood ARTIs of viral origin is responsible for spreading resistant microbial strains and thereby increasing the disease burden [29]. These findings are comparable with a Jordanian study in which penicillins and cephalosporins were prescribed to a large proportion of the pediatric population [30]. In contrast to developing countries, the rate of antibiotic prescribing among ARTI patients declined from 5.2 to 2.2 prescription per 1000 pediatric patients during the last decade in various states of the UK [31]. In Pakistan, a survey-based study at a national level revealed that ARTIs were the most common indications for prescribing antibiotics and that, in most of the cases, the prescribing practices of many healthcare professionals were irrational [32].
Like the previously published literature [33,34,35], the present study also revealed that antibiotics were more frequently prescribed to patients who had long LOS in hospital compared to those who had short LOS. Most of the ARTIs (such as bronchitis) are of viral origin, and the IDSP guidelines recommend limited use of antibiotics. However, prescribers are compelled to prescribe antibiotics because of their inability to differentiate between viral and bacterial infections; parental demand to prescribe antibiotics; socioeconomic pressures; and to reduce the risk of secondary bacterial infections, duration of cough, and other symptoms [36,37,38]. The noncompliance of these guidelines was also observed in the present study. Macrolides were frequently prescribed in bronchitis, which can be managed through symptomatic treatment. In cases of pneumonia, ampicillin was prescribed as 57 mg/kg/day three times a day instead of 100 mg/kg/day four times a day [39]. These irrational practices are also attributed to the fact that, in Pakistan, pharmacists have a major role in procurement and dispensing of medicines but have limited exposure to the clinical setup and direct patient care. To implement rational antibiotic prescribing practices, the establishment of an antibiotic prescribing surveillance system and continual medical education programs need to be immediately implemented. In case of the pediatric population, clinical pharmacists must participate in parental counseling training programs of healthcare professionals.

4.2. Antibiotic Prescribing Errors

The present study revealed that most of the prescribing errors were related to wrong dose (especially underdosing), wrong frequency (especially prescribed greater than the recommended frequency), and duplicate therapy, particularly in the records of patients who had long LOS compared to those who had short LOS. These findings are in line with a retrospective study conducted on Brazilian pediatric patients in which long LOS was found in patients who had been prescribed with antibiotics [40]. Similarly, a prospective study depicted that higher rate of dosing errors in the medication record can threaten patient safety, especially in the pediatric population, because dose calculation is often more complex for these patients [41]. Wrong dose and frequency errors were commonly found among pediatric patients because many of the antibiotics were not readily available in pediatric unit doses, and pediatric doses were therefore calculated from adult unit doses. Antibiotic prescribing errors that are related to their frequent use may not only economically burden the healthcare system by increasing the patient’s LOS in hospital but also subsequently play a crucial role in spreading antibiotic-resistant microbial strains [42]. Nonadherence to national and international guidelines and national formularies for the pediatric population could be the possible causes of these errors [15]. Therefore, hospital formularies and international standard treatment guidelines for pediatrics must be made available in all healthcare settings. To overcome the irrational prescribing of antibiotics, strict diagnostic criteria must be established for ARTIs of bacterial origin. The government must ensure availability of adequate number of hospital and clinical pharmacists in all pediatric public healthcare settings. Their prime responsibilities must include prescription evaluation, calculation of doses, reporting of antibiotic prescribing errors, and counseling of parents about the proper use of antibiotics. Moreover, the Pakistan Pediatric Association (PPA) must take initiatives to develop and implement Pakistan’s own national formulary for pediatrics so that countrywide uniform treatment protocols are established.
The inadequate healthcare system for pediatric patients has led to an increased incidence of prescribing errors and child mortalities. Low state spending on child health, abject poverty, and low literacy rate of parents has indirectly worsened the healthcare system in Pakistan [43]. Therefore, it is recommended that medical and paramedical staff members, along with senior consultants, are increased with the increase in patient load so that each patient gets adequate consultation time, and the risk of prescribing errors are reduced.

4.3. Factors Associated with Prescribing Errors

The prescribing errors were less likely to be found in the record of female patients. These findings are in line with previously published studies conducted in different states of Saudi Arabia and Pakistan, where pediatric male gender showed a greater association with prescribing errors [17,44]. Contrary to this, a meta-analysis showed that females were more susceptible to encountering prescribing errors than males [45]. Pakistan is an economically less developed country, where no public child healthcare insurance policy is available. Parents have to bear the health expense of their children on their own, and financial constraints and social norms compel most of the low-income households to prefer medical treatment for male children compared to female children. Due to this reason, male pediatric patients are more likely to be admitted in inpatient settings and are thus at higher risk of encountering prescribing errors than females [46].
Similar to previously published studies [47,48,49], LOS was found to be a significant factor for prescribing error. This might be due to the fact patients were prescribed with more number of antibiotics during their prolonged stay in the inpatient departments, which increased the risk of encountering antibiotic prescribing errors. Prescribing errors were more likely to be found in the records of patients suffering from URTIs compared to sufferers of LRTIs. These findings are consistent with previously published studies, where prescribing errors were less commonly found in the prescription records of patients suffering from LRTIs [50,51,52]. This may be attributed to the fact that LRTIs (like pneumonia) are more prevalent in the pediatric population than any URTIs, so specialized medical care is being provided to patients suffering from LRTIs. The prime focus of the available guidelines (such as the IDSP guidelines) is the management of LRTIs because, in most of cases, URTIs are usually mild and self-limiting [53]. Furthermore, statistical analysis revealed significant association between >3 prescribed antibiotics and higher risk of prescribing errors. These findings are consistent with previously published studies, which have shown that the number of antibiotics on prescription is a strong predictor of prescribing error in such a way that the risk of error becomes several folds with the addition of a single antibiotics in prescription [54,55,56]. This may be attributed to various reasons, including diagnostic uncertainties reflecting the physician’s inability to distinguish between viral and bacterial infections, noncompliance of guidelines, poor practices of antimicrobial stewardship (AMS) program, heavy patient load, and unreasonable patient demands on physicians to prescribe antibiotics [57,58,59].

5. Strengths and limitations

To the best of our knowledge, this is the first study that deals with antibiotic prescribing errors among pediatric inpatients suffering from ARTIs. These findings will be beneficial to stakeholders in establishing policies and procedures for prescribing antibiotics to children aged 0−9 years. This study emphasized the need for an antibiotic prescribing errors reporting system, a national survey demonstrating rational use of antibiotics among the pediatric population, and the development and implementation of Pakistan own national formulary for pediatrics.
As with any study, this study also has limitations. First, the results cannot be generalized for Pakistan as a whole because clustering of data at different levels was not taken into account, and multilevel modeling was also not performed to test associated factors. Therefore, antibiotic prescribing practices may vary due to geographic variation of the selected healthcare settings, the prescribing habits of physicians, and the clustering effect. However, the healthcare sector conditions are similar across many regions of the country, and physicians consequently follow the same prescribing practices. We suspect that the findings and the issues raised will be similar in “like” hospitals (i.e., tertiary-care hospitals), so there are relevant learnings for the tertiary sector in Pakistan. Second, as this was a cross-sectional study, it was not possible to see the outcomes of antibiotic prescribing errors, i.e., adverse events and mortalities. Third, the findings of the present study are limited to pediatric patients suffering from only ARTIs because the inclusion of other ARTIs would have complicated the findings. Clinically based longitudinal studies may help to overcome these limitations.

6. Conclusions

The present study concluded that penicillins, macrolides, and cephalosporins were frequently prescribed classes of antibiotics in ARTIs, especially in the prescription records of patients who had long LOS. Among these, ampicillin, amoxicillin, azithromycin, and ceftriaxone were the most commonly prescribed agents. Prescription errors like underdosing, high frequency, and duplicate therapy were most commonly found among records of patients who suffered from LRTIs and were admitted for long periods of time in the public hospitals of Lahore. Caution must be exercised in prescribing antibiotics to the pediatric population because antibiotic prescribing errors can be hazardous to lives.

Supplementary Materials

The following are available online at https://www.mdpi.com/1648-9144/55/2/44/s1.

Author Contributions

Conceptualization, M.R.S.; methodology, M.R.S.; formal analysis, S.I. and A.S.; investigation, S.I. and A.S.; writing—original draft preparation, S.I. and A.S.; writing—review and editing, M.R.S., S.I., A.S., M.S. and Q.-u.-a.-S.; supervision, M.R.S.

Funding

No funding was involved in the preparation of this manuscript or in the decision to submit it for publication.

Acknowledgments

We would like to express our wholehearted thanks to the administrations of all the selected settings of Lahore, Pakistan. We express gratitude to Shane Scahill (Senior Lecturer, Massey University, New Zealand) for reviewing and editing the paper and for valuable comments. Also, a note of thanks to all pharmacy students who acted as data collectors.

Conflicts of Interest

The authors declare that they have no competing interests.

Availability of data and material

The raw data on which conclusions of this manuscript rely is available upon request. Please contact Muhammad Rehan Sarwar at [email protected].

References

  1. Simoes, E.A.; Cherian, T.; Chow, J.; Shahid-Salles, S.A.; Laxminarayan, R.; John, T.J. Acute respiratory infections in children. In Disease Control Priorities in Developing Countries, 2nd ed.; Jamison, D.T., Breman, J.G., Measham, A.R., Alleyne, G., Claeson, M., Evans, D.B., Jha, P., Mills, A., Musgrove, P., Eds.; Oxford University Press: Washington, DC, USA, 2006. [Google Scholar]
  2. Montasser, N.; Helal, R.; Rezq, R. Assessment and classification of acute respiratory tract infections among Egyptian rural children. Br. J. Med. Med. Res. 2012, 2, 216. [Google Scholar] [CrossRef]
  3. Vikaspedia. Acute respiratory infection(ARI). Available online: http://vikaspedia.in/health/diseases/lungs-related/acute-respiratory-infection-ari (accessed on 12 January 2019).
  4. Rudan, I.; Tomaskovic, L.; Boschi-Pinto, C.; Campbell, H. Global estimate of the incidence of clinical pneumonia among children under five years of age. Bull. World Health Organ. 2004, 82, 895–903. [Google Scholar] [PubMed]
  5. Vashishtha, V.M. Current status of tuberculosis and acute respiratory infections in India: Much more needs to be done! Indian Pediatr. 2010, 47, 88–89. [Google Scholar] [CrossRef] [PubMed]
  6. Economics, T. Pakistan—Prevalence of acute respiratory infection (ARI) (% of children under 5). Available online: https://tradingeconomics.com/pakistan/prevalence-of-acute-respiratory-infection-ari-percent-of-children-under-5-q3-wb-data.html (accessed on 12 January 2019).
  7. Alumran, A.; Hurst, C.; Hou, X.-Y. Antibiotics overuse in children with upper respiratory tract infections in Saudi Arabia: Risk factors and potential interventions. Clin. Med. Diagn. 2011, 1, 8–16. [Google Scholar] [CrossRef]
  8. Mangione-Smith, R.; Zhou, C.; Robinson, J.D.; Taylor, J.A.; Elliott, M.N.; Heritage, J. Communication practices and antibiotic use for acute respiratory tract infections in children. Ann. Family Med. 2015, 13, 221–227. [Google Scholar] [CrossRef]
  9. Sarwar, M.R.; Saqib, A.; Iftikhar, S.; Sadiq, T. Antimicrobial use by WHO methodology at primary health care centers: A cross sectional study in Punjab, Pakistan. BMC Infect. Dis. 2018, 18, 492. [Google Scholar] [CrossRef]
  10. Ayukekbong, J.A.; Ntemgwa, M.; Atabe, A.N. The threat of antimicrobial resistance in developing countries: Causes and control strategies. Antimicrob. Resist. Infect. Control 2017, 6, 47. [Google Scholar] [CrossRef]
  11. Aabenhus, R.; Hansen, M.P.; Saust, L.T.; Bjerrum, L. Characterisation of antibiotic prescriptions for acute respiratory tract infections in Danish general practice: A retrospective registry based cohort study. NPJ Prim. Care Respir. Med. 2017, 27, 37. [Google Scholar] [CrossRef]
  12. Ali, S.R.; Ahmed, S.; Lohana, H. Trends of empiric antibiotic usage in a secondary care hospital, Karachi, Pakistan. Int. J. Pediatr. 2013, 832857. [Google Scholar] [CrossRef]
  13. Dean, B.; Schachter, M.; Vincent, C.; Barber, N. Prescribing errors in hospital inpatients: their incidence and clinical significance. Qual. Saf. Health Care 2002, 11, 340–344. [Google Scholar] [CrossRef]
  14. Sarwar, M.R.; Saqib, A.; Iftikhar, S.; Sadiq, T. Antimicrobial use by WHO methodology at primary health care centers: A cross sectional study in Punjab, Pakistan. BMC Infect. Dis. 2018, 18, 492. [Google Scholar] [CrossRef]
  15. Khalil, S.; Toor, K.M.; Khan, H.S. Irrational Use of Antibiotics in Children. Pakistan Pediatr. J. 2015, 39, 131–139. [Google Scholar]
  16. Zeleke, A.; Chanie, T.; Woldie, M. Medication prescribing errors and associated factors at the pediatric wards of Dessie Referral Hospital, Northeast Ethiopia. Int. Arch. Med. 2014, 7, 18. [Google Scholar] [CrossRef]
  17. Al-Jeraisy, M.I.; Alanazi, M.Q.; Abolfotouh, M.A. Medication prescribing errors in a pediatric inpatient tertiary care setting in Saudi Arabia. BMC Res. Notes 2011, 4, 294. [Google Scholar] [CrossRef]
  18. The Newspaper’s Staff Reporter. Medication Errors Cause Half a Million Deaths in Pakistan, Say Pharmacists. Dawn, 11 October 2017. [Google Scholar]
  19. Kozer, E. Medication errors in children. Paediatr. Drugs 2009, 11, 52–54. [Google Scholar] [CrossRef]
  20. World Health Organization. International Classification of Primary Care (ICPC-2); WHO: Geneva, Switzerland, 2011. [Google Scholar]
  21. World Health Organization. The Anatomical Therapeutic Chemical Classification System with Defined Daily Doses (ATC/DDD); WHO: Oslo, Norway, 2006. [Google Scholar]
  22. Average Length of Stay in Hospitals; Pennsylvania Department of Health: Harrisburg, PA, USA, 2014.
  23. McPhee, S.J.; Papadakis, M.A.; Tierney, L.M. Current Medical Diagnosis & Treatment 2010; McGraw-Hill Medical: New York, NY, USA, 2010. [Google Scholar]
  24. Committee, P.F. BNF for Children 2014–2015 (BNFC); Pharmaceutical Press: London, UK, 2014. [Google Scholar]
  25. Tan, T.; Little, P.; Stokes, T. Antibiotic prescribing for self limiting respiratory tract infections in primary care: summary of NICE guidance. BMJ: Br. Med. J. 2008, 337, a437. [Google Scholar] [CrossRef]
  26. Mandell, L.A.; Wunderink, R.G.; Anzueto, A.; Bartlett, J.G.; Campbell, G.D.; Dean, N.C.; Dowell, S.F.; File, T.M., Jr.; Musher, D.M.; Niederman, M.S. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin. Infect. Dis. 2007, 44, S27–S72. [Google Scholar] [CrossRef]
  27. Infectious Disease Society of Pakistan. Guidelines for the Use of Antmicrobials; Infectious Disease Society of Pakistan: Karachi, Pakistan, 2007. [Google Scholar]
  28. Rogawski, E.T.; Platts-Mills, J.A.; Seidman, J.C.; John, S.; Mahfuz, M.; Ulak, M.; Shrestha, S.K.; Soofi, S.B.; Yori, P.P.; Mduma, E. Use of antibiotics in children younger than two years in eight countries: A prospective cohort study. Bull. World Health Organ. 2017, 95, 49. [Google Scholar] [CrossRef]
  29. Hameed, A.; Naveed, S.; Qamar, F.; Alam, T.; Abbas, S. Irrational Use of Antibiotics. Different Age Groups of Karachi: A Wakeup Call for Antibiotic Resistance and Future Infections. J. Bioequiv. Availab. 2016, 8, 242–245. [Google Scholar]
  30. Ababneh, M.A.; Al-Azzam, S.I.; Ababneh, R.; Rababa’h, A.M.; Demour, S.A. Antibiotic prescribing for acute respiratory infections in children in Jordan. Int. Health 2017, 9, 124–130. [Google Scholar] [CrossRef]
  31. Meropol, S.B.; Chen, Z.; Metlay, J.P. Reduced antibiotic prescribing for acute respiratory infections in adults and children. Br. J. Gen. Pract. 2009, 59, e321–e328. [Google Scholar] [CrossRef]
  32. Taufiq, M.; Zuberi, R.W. Overuse of antibiotics In children for upper respiratory infections (URIs): A Dilemma. J. Coll. Phys. Surg. Pak. 2011, 21, 59–60. [Google Scholar]
  33. Landstedt, K.; Sharma, A.; Johansson, F.; Lundborg, C.S.; Sharma, M. Antibiotic prescriptions for inpatients having non-bacterial diagnosis at medicine departments of two private sector hospitals in Madhya Pradesh, India: A cross-sectional study. BMJ Open 2017, 7, e012974. [Google Scholar] [CrossRef]
  34. Sharma, M.; Damlin, A.L.; Sharma, A.; Stålsby Lundborg, C. Antibiotic prescribing in medical intensive care units–a comparison between two private sector hospitals in Central India. Infect. Dis. 2015, 47, 302–309. [Google Scholar] [CrossRef]
  35. Sharma, M.; Eriksson, B.; Marrone, G.; Dhaneria, S.; Lundborg, C.S. Antibiotic prescribing in two private sector hospitals; one teaching and one non-teaching: A cross-sectional study in Ujjain, India. BMC Infect. Dis. 2012, 12, 155. [Google Scholar] [CrossRef]
  36. Smith, S.M.; Smucny, J.; Fahey, T. Antibiotics for acute bronchitis. JAMA 2014, 312, 2678–2679. [Google Scholar] [CrossRef]
  37. Cotton, M.F.; Innes, S.; Jaspan, H.; Madide, A.; Rabie, H. Management of upper respiratory tract infections in children. S. Afr. Family Pract. 2008, 50, 6–12. [Google Scholar] [CrossRef]
  38. Bartlett, J.G.; Gilbert, D.N.; Spellberg, B. Seven ways to preserve the miracle of antibiotics. Clin. Infec. Dis. 2013, 56, 1445–1450. [Google Scholar] [CrossRef]
  39. Zoorob, R.; Sidani, M.A.; Fremont, R.D.; Kihlberg, C. Antibiotic use in acute upper respiratory tract infections. Am. Family Phys. 2012, 8, 810–816. [Google Scholar]
  40. Carneiro, M.; Ferraz, T.; Bueno, M.; Koch, B.E.; Foresti, C.; Lena, V.F.; Machado, J.A.; Rauber, J.M.; Krummenaauer, E.C.; Lazaroto, D.M. Antibiotic prescription in a teaching hospital: A brief assessment. Revista da Associação Médica Brasileira 2011, 57, 421–424. [Google Scholar] [CrossRef]
  41. Glanzmann, C.; Frey, B.; Meier, C.R.; Vonbach, P. Analysis of medication prescribing errors in critically ill children. Eur. J. Pediatr. 2015, 174, 1347–1355. [Google Scholar] [CrossRef]
  42. Walsh, K.E.; Kaushal, R.; Chessare, J.B. How to avoid paediatric medication errors: A user’s guide to the literature. Arch. Dis. Child. 2005, 90, 698–702. [Google Scholar] [CrossRef]
  43. Shahid, D.H.A. Child healthcare in Pakistan. Dawn, 25 September 2012. [Google Scholar]
  44. Khayam, M.U. Medication Errors Assessment and Prevention by a Clinical Pharmacist in Pediatric Wards of RMI Hospital Peshawar, KPK-Pakistan. Ann. Pak. Inst. Med. Sci 2015, 11, 124–129. [Google Scholar]
  45. Schröder, W.; Sommer, H.; Gladstone, B.P.; Foschi, F.; Hellman, J.; Evengard, B.; Tacconelli, E. Gender differences in antibiotic prescribing in the community: A systematic review and meta-analysis. J. Antimicrob. Chemother. 2016, 71, 1800–1806. [Google Scholar] [CrossRef]
  46. Ali, S.M. Gender and health care utilisation in Pakistan. Pak. Dev. Rev. 2000, 213–234. [Google Scholar] [CrossRef]
  47. Sheikh, D.; Mateti, U.V.; Kabekkodu, S.; Sanal, T. Assessment of medication errors and adherence to WHO prescription writing guidelines in a tertiary care hospital. Future J. Pharm. Sci. 2017, 3, 60–64. [Google Scholar] [CrossRef]
  48. Lesar, T.S.; Lomaestro, B.M.; Pohl, H. Medication-prescribing errors in a teaching hospital. A 9-year experience. Arch. Intern. Med. 1997, 157, 1569–1576. [Google Scholar] [CrossRef]
  49. Horace, A.E.; Ahmed, F. Polypharmacy in pediatric patients and opportunities for pharmacists’ involvement. Integr. Pharm. Res. Pract. 2015, 4, 113–126. [Google Scholar] [CrossRef]
  50. Leblebicioglu, H.; Canbaz, S.; Peksen, Y.; Gunaydin, M. Physicians’ antibiotic prescribing habits for upper respiratory tract infections in Turkey. J. Chemother. 2002, 14, 181–184. [Google Scholar] [CrossRef]
  51. Ball, P.; Baquero, F.; Cars, O.; File, T.; Garau, J.; Klugman, K.; Low, D.; Rubinstein, E.; Wise, R.; Resistance, C.G.o.; et al. Antibiotic therapy of community respiratory tract infections: Strategies for optimal outcomes and minimized resistance emergence. J. Antimicrob. Chemother. 2002, 49, 31–40. [Google Scholar] [CrossRef]
  52. Dosh, S.A.; Hickner, J.M.; Mainous, A.G.I.; Ebell, M.H. Predictors of antibiotic prescribing for nonspecific upper respiratory infections, acute bronchitis, and acute sinusitis. J. Family Pract. 2000, 49, 407. [Google Scholar]
  53. Losier, A.; Britto-Leon, C.; Cruz, C.S.D. General Approach to the Patient with a Respiratory Infection. Available online: https://www.pulmonologyadvisor.com/pulmonary-medicine/general-approach-to-the-patient-with-a-respiratory-infection/article/661003/. (accessed on 16 January 2019).
  54. Zhang, Z.; Hu, Y.; Zou, G.; Lin, M.; Zeng, J.; Deng, S.; Zachariah, R.; Walley, J.; Tucker, J.D.; Wei, X. Antibiotic prescribing for upper respiratory infections among children in rural China: A cross-sectional study of outpatient prescriptions. Glob. Health Action 2017, 10, 1287334. [Google Scholar] [CrossRef]
  55. Donelan, K.; Hill, C.A.; Hoffman, C.; Scoles, K.; Feldman, P.H.; Levine, C.; Gould, D. Challenged to care: Informal caregivers in a changing health system. Health Aff. 2002, 21, 222–231. [Google Scholar] [CrossRef]
  56. Seden, K.; Kirkham, J.J.; Kennedy, T.; Lloyd, M.; James, S.; Mcmanus, A.; Ritchings, A.; Simpson, J.; Thornton, D.; Gill, A. Cross-sectional study of prescribing errors in patients admitted to nine hospitals across North West England. BMJ Open 2013, 3, e002036. [Google Scholar] [CrossRef]
  57. Williams, A.; Mathai, A.S.; Phillips, A.S. Antibiotic prescription patterns at admission into a tertiary level intensive care unit in Northern India. J. Pharm. Bioallied Sci. 2011, 3, 531. [Google Scholar] [CrossRef]
  58. Shahid, A.; Iftikhar, F.; Arshad, M.K.; Javed, Z.; Sufyan, M.; Ghuman, R.S.; Tarar, Z. Knowledge and attitude of physicians about antimicrobial resistance and their prescribing practices in Services hospital, Lahore, Pakistan. J. Pak. Med. Assoc. 2017, 67, 968. [Google Scholar]
  59. Sarwar, M.R.; Saqib, A.; Iftikhar, S.; Sadiq, T. Knowledge of community pharmacists about antibiotics, and their perceptions and practices regarding antimicrobial stewardship: A cross-sectional study in Punjab, Pakistan. Infect. Drug Resist. 2018, 11, 133. [Google Scholar] [CrossRef]
Table
Table 1. Characteristics of the patients.
Table 1. Characteristics of the patients.
CharacteristicsInpatients (n = 11,852)URTIs * (n = 2036)LRTIs † (n = 9816)p-Value
GenderMale7481 (63.1)1219 (59.9)6262 (63.8)<0.001
Female4371 (36.9)817 (40.1)3554 (36.2)
Age0–3 years4781 (40.4)894 (43.9)3887 (39.6)
4–6 years4697 (39.6)662 (32.5)4035 (41.1)<0.001
7–9 years2374 (20.0)480 (23.6)1894 (19.3)
Weight3–10 kg5202 (43.9)803 (39.4)4399 (44.8)
11–18 kg3902 (32.9)851 (41.8)3051 (31.1)<0.001
≥19 kg2748 (23.2)382 (18.8)2366 (24.1)
Number of antibiotics prescribed per prescription1205 (1.8)98 (4.8)107 (1.1)
26433 (54.1)1109 (54.5)5324 (54.2)<0.001
≥35214 (44.1)829 (40.7)4385 (44.7)
LOSShort (mean = 3.7, range 1–4)5567 (47.0)958 (47.1)4609 (46.9)
Long (mean = 6.6, range 5–14)6285 (53.0)1078 (52.9)5207 (53.1)<0.001
* URTIs = upper respiratory tract infections; † LRTIs = lower respiratory tract infections; LOS = length of stay.
Table
Table 2. Prescribing pattern of antibiotics among the study population.
Table 2. Prescribing pattern of antibiotics among the study population.
AntibioticsATC coden (%)URTIs LRTIs
Total (3500)Short LOS (1675)Long LOS (1826)Total (23,383)Short LOS (10,993)Long LOS (12,392)
GentamycinJ01GB033114 (11.6)---------3114 (13.3)1439 (13.1)1675 (13.5)
AmoxicillinJ01CA047854 (29.2)584 (16.7)294 (17.6)290 (15.9)7270 (31.1)3359 (30.6)3911 (31.6)
AmpicillinJ01CA015743 (21.4)101 (2.9)38 (2.3)63 (3.5)5642 (24.1)2621 (23.8)3021 (24.4)
Co-amoxiclavJ01CA04499 (1.9)499 (14.3)222 (13.3)277 (15.2)---------
ClarithromycinJ01FA09540 (2.0)273 (7.8)146 (8.7)127 (6.9)267 (1.1)149 (1.4)118 (0.9)
AzithromycinJ01FA101559 (5.8)333 (9.5)176 (10.5)157 (8.6)1226 (5.2)589 (5.4)637 (5.1)
ErythromycinJ01FA01305 (1.1)90 (2.6)43 (2.6)47 (2.6)215 (0.9)120 (1.1)95 (0.8)
CefiximeJ01DD0869 (0.2)69 (1.9)31 (1.9)38 (2.1)---------
CefuroximeJ01DC0288 (0.3)88 (2.5)38 (2.3)50 (2.7)---------
CefadroxilJ01DB05103 (0.4)103 (2.9)59 (3.5)44 (2.4)---------
CefotaximeJ01DA10746 (2.8)207 (5.9)88 (5.3)119 (6.5)539 (2.3)281 (2.6)258 (2.1)
CephalexinJ01DB01186 (0.7)186 (5.3)106 (6.3)80 (4.4)---------
CeftriaxoneJ01DA133314 (12.3)517 (14.8)225 (13.4)292 (16.0)2797 (11.9)1335 (12.2)1462 (11.8)
LevofloxacinJ01MA12907 (3.4)77 (2.2)34 (2.0)43 (2.4)830 (3.5)383 (3.5)447 (3.6)
CiprofloxacinJ01MA02151 (0.6)---------151 (0.6)79 (0.7)72 (0.6)
ClindamycinJ01FF01975 (3.6)218 (6.2)109 (6.5)109 (5.9)757 (3.2)360 (3.3)397 (3.2)
MeropenemJ01DH0212 (0.1)12 (0.3)5 (0.3)7 (0.4)---------
VancomycinJ01XA01679 (2.5)104 (2.9)44 (2.6)60 (3.3)575 (2.5)276 (2.5)299 (2.4)
LinezolidJ01XX0839 (0.2)39 (1.1)17 (1.1)22 (1.2)---------
LOS = length of stay; LRTIs = lower respiratory tract infections; URTIs = upper respiratory tract infections.
Table
Table 3. Antibiotic prescribing errors among pediatric patients in Lahore, Pakistan.
Table 3. Antibiotic prescribing errors among pediatric patients in Lahore, Pakistan.
DiseasesPatients n (%)Prescribing Errors
Irrational Prescribing n (%)Wrong Drug n (%) Wrong Dose n (%)Wrong Frequency n (%)Wrong Duration n (%) Wrong Route n (%)Duplicate Therapy n (%)
Over Dose Underdose HighLow
LRTIs
Pneumonia8786 (89.5)3102 (35.3)404 (13.0)185 (5.9)435 (14.0)341 (10.9)248 (7.9)494 (14.9)433 (13.9)562 (18.1)
Epiglottitis731 (7.5)488 (66.8)62 (12.7)42 (8.6)55 (11.3)54 (11.1)39 (7.9)81 (16.6)71 (14.6)84 (17.2)
Bronchitis299 (3.1)132 (44.1)19 (14.4)8 (6.1)19 (14.4)16 (12.1)8 (6.0)19 (14.4)15 (11.4)28 (21.2)
Total LRTIs9816 (82.8)3722 (37.9)485 (13.0)235 (6.3) 509 (13.7)411 (11.0)295 (7.9)594(15.9)519(13.9)674(18.1)
744 (19.9)706 (18.9)
URTIs
Tonsillitis and pharyngitis608 (29.9)384 (63.1)48 (12.5)20 (5.2)57 (14.8)42 (10.9)32 (8.3)63 (17.0)57 (14.8)65 (16.9)
Common cold123 (6.0)58 (47.2)7 (12.1)6 (10.3)6 (10.3)7 (12.1)3 (5.2)9 (15.5)10 (17.2)10 (17.2)
Whooping cough171 (8.4)121 (70.7) 16 (13.2)7 (5.8)17 (14.0)16 (13.2)7 (5.8)19 (15.7)17 (14.0)22 (18.2)
Acute bacterial sinusitis577 (28.3)230 (39.9)31 (13.5)13 (5.7)33 (14.3)29 (12.6)14 (6.0)35 (15.2)29 (12.6)46 (20.0)
Bacterial tracheitis155 (7.6)128 (82.6)15 (11.7)9 (7.0)17 (13.3)12 (9.4)13 (10.2)22 (17.2)21 (16.4)19 (14.8)
Laryngitis and croup402 (19.8)193 (48.0)27 (13.9)12 (6.2)26 (13.5)24 (12.4)12 (6.2)29 (15.0)24 (12.4)39 (20.2)
Total URTIs2036 (17.2)1114 (54.7)144 (12.9)67 (6.0)156 (14.0)130 (11.7)81 (7.3)177 (15.9)158 (14.2)201 (18.0)
223 (20.0)211 (18.9)
Overall Total11,8524836 (40.8)629 (13.0)302 (6.2)665 (13.8)541 (11.2)376 (7.8)771 (15.9)677 (13.9)875 (18.1)
967 (19.9)917 (18.9)
LRTIs = lower respiratory tract infections; URTIs = upper respiratory tract infections; LOS = length of stay.
Table
Table 4. Logistic regression analysis of factors associated with prescribing errors.
Table 4. Logistic regression analysis of factors associated with prescribing errors.
CharacteristicsOR95% CIp-Value
GenderMale ------
Female0.60.1–0.90.012
AgeNewborn to toddler (0–3 years) ------------
Preschooler (4–6 years)0.40.01–1.10.210
School aged child (7–9 years)0.80.5–1.40.167
Weight3–10 kg ------------
11–18 kg0.70.3–1.20.430
≥19 kg0.60.4–1.90.367
Number of antibiotics prescribed per prescription1 ------------
20.90.3–1.60.321
≥31.71.0–2.10.020
LOSShort (<5 days) ------------
Long (≥5 days)12.510.1–17.6<0.001
ARTIsURTIs2.81.7–3.9<0.001
LRTIs -------------
OR: odd ratio; CI: confidence Interval; LOS: length of stay; ARTIs: acute respiratory tract infections; URTIs: upper respiratory tract infections; LRTIs: lower respiratory tract infections.

Share and Cite

MDPI and ACS Style

Iftikhar, S.; Sarwar, M.R.; Saqib, A.; Sarfraz, M.; Shoaib, Q.-u.-a. Antibiotic Prescribing Practices and Errors among Hospitalized Pediatric Patients Suffering from Acute Respiratory Tract Infections: A Multicenter, Cross-Sectional Study in Pakistan. Medicina 2019, 55, 44. https://doi.org/10.3390/medicina55020044

AMA Style

Iftikhar S, Sarwar MR, Saqib A, Sarfraz M, Shoaib Q-u-a. Antibiotic Prescribing Practices and Errors among Hospitalized Pediatric Patients Suffering from Acute Respiratory Tract Infections: A Multicenter, Cross-Sectional Study in Pakistan. Medicina. 2019; 55(2):44. https://doi.org/10.3390/medicina55020044

Chicago/Turabian Style

Iftikhar, Sadia, Muhammad Rehan Sarwar, Anum Saqib, Muhammad Sarfraz, and Qurat-ul-ain Shoaib. 2019. "Antibiotic Prescribing Practices and Errors among Hospitalized Pediatric Patients Suffering from Acute Respiratory Tract Infections: A Multicenter, Cross-Sectional Study in Pakistan" Medicina 55, no. 2: 44. https://doi.org/10.3390/medicina55020044

Article Metrics

Back to TopTop