<?xml version="1.0" encoding="UTF-8"?><!DOCTYPE article  PUBLIC "-//NLM//DTD Journal Publishing DTD v3.0 20080202//EN" "http://dtd.nlm.nih.gov/publishing/3.0/journalpublishing3.dtd"><article xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" dtd-version="3.0" xml:lang="en" article-type="research article"><front><journal-meta><journal-id journal-id-type="publisher-id">PP</journal-id><journal-title-group><journal-title>Pharmacology &amp; Pharmacy</journal-title></journal-title-group><issn pub-type="epub">2157-9423</issn><publisher><publisher-name>Scientific Research Publishing</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="doi">10.4236/pp.2022.1310029</article-id><article-id pub-id-type="publisher-id">PP-120529</article-id><article-categories><subj-group subj-group-type="heading"><subject>Articles</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Chemistry&amp;Materials Science</subject><subject> Medicine&amp;Healthcare</subject></subj-group></article-categories><title-group><article-title>
 
 
  Antibiotic Prescribing Patterns in Adult Patients According to the WHO AWaRe Classification: A Multi-Facility Cross-Sectional Study in Primary Healthcare Hospitals in Lusaka, Zambia
 
</article-title></title-group><contrib-group><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Steward</surname><given-names>Mudenda</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Mary</surname><given-names>Chomba</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Billy</surname><given-names>Chabalenge</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Christabel</surname><given-names>Nang’andu Hikaambo</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Michelo</surname><given-names>Banda</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Victor</surname><given-names>Daka</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Annie</surname><given-names>Zulu</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Abraham</surname><given-names>Mukesela</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Maxwell</surname><given-names>Kasonde</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Peter</surname><given-names>Lukonde</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Enock</surname><given-names>Chikatula</given-names></name><xref ref-type="aff" rid="aff6"><sup>6</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Lloyd</surname><given-names>Matowe</given-names></name><xref ref-type="aff" rid="aff7"><sup>7</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Ronald</surname><given-names>Kampamba Mutati</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Tyson</surname><given-names>Lungwani Muungo</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Tobela</surname><given-names>Mudenda</given-names></name><xref ref-type="aff" rid="aff8"><sup>8</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Shafiq</surname><given-names>Mohamed</given-names></name><xref ref-type="aff" rid="aff9"><sup>9</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Scott</surname><given-names>Matafwali</given-names></name><xref ref-type="aff" rid="aff10"><sup>10</sup></xref></contrib></contrib-group><aff id="aff2"><addr-line>Department of Medicines Control, Zambia Medicines Regulatory Authority, Lusaka, Zambia</addr-line></aff><aff id="aff6"><addr-line>Department of Pharmacy, Levy Mwanawasa University Teaching Hospital, Lusaka, Zambia</addr-line></aff><aff id="aff5"><addr-line>Ministry of Health Headquarters, Ndeke House, Lusaka, Zambia</addr-line></aff><aff id="aff1"><addr-line>Department of Pharmacy, School of Health Sciences, University of Zambia, Lusaka, Zambia</addr-line></aff><aff id="aff8"><addr-line>Department of Pathology, Ndola Teaching Hospital, Ndola, Zambia</addr-line></aff><aff id="aff7"><addr-line>Faculty of Pharmacy, School of Pharmacy, Eden University, Lusaka, Zambia</addr-line></aff><aff id="aff4"><addr-line>Bell Pharmacy, Kabulonga Centro Mall, Lusaka, Zambia</addr-line></aff><aff id="aff10"><addr-line>Clinical Research Department, Faculty of Infectious and Tropical Diseases, London School of Hygiene &amp;amp; Tropical Medicine, London, UK</addr-line></aff><aff id="aff9"><addr-line>Remedium Pharmaceuticals Limited, Lusaka, Zambia</addr-line></aff><aff id="aff3"><addr-line>Department of Public Health, Michael Chilufya Sata School of Medicine, Copperbelt University, Ndola, Zambia</addr-line></aff><pub-date pub-type="epub"><day>10</day><month>10</month><year>2022</year></pub-date><volume>13</volume><issue>10</issue><fpage>379</fpage><lpage>392</lpage><history><date date-type="received"><day>1,</day>	<month>September</month>	<year>2022</year></date><date date-type="rev-recd"><day>16,</day>	<month>October</month>	<year>2022</year>	</date><date date-type="accepted"><day>19,</day>	<month>October</month>	<year>2022</year></date></history><permissions><copyright-statement>&#169; Copyright  2014 by authors and Scientific Research Publishing Inc. </copyright-statement><copyright-year>2014</copyright-year><license><license-p>This work is licensed under the Creative Commons Attribution International License (CC BY). http://creativecommons.org/licenses/by/4.0/</license-p></license></permissions><abstract><p>
 
 
  Introduction: Indiscriminate prescribing and using of antibiotics have led to the development of antimicrobial resistance (AMR). To reduce this problem, the World Health Organization (WHO) developed the “Access”, “Watch”, and “Reserve” (AWaRe) classification of antibiotics that promotes antimicrobial stewardship (AMS). In Zambia, there are gaps in practice regarding prescribing of antibiotics based on the AWaRe protocol. This study assessed antibiotic prescribing patterns in adult in-patients in selected primary healthcare hospitals in Lusaka, Zambia. 
  Materials and Methods: This retrospective cross-sectional study was conducted using 388 patient medical files from September 2021 to November 2021, five primary healthcare hospitals namely; Chawama, Matero, Chilenje, Kanyama, and Chipata. Data analysis was performed using the Statistical Package for Social Sciences version 23. 
  Results: Of the selected medical files, 52.3% (n = 203) were for male patients. Overall, the prevalence of antibiotic use was 82.5% (n = 320) which was higher than the WHO recommendation of a less than 30% threshold. The most prescribed antibiotic was ceftriaxone (20.3%), a Watch group antibiotic, followed by metronidazole (17.8%) and sulfamethoxazole/trimethoprim (16.3%), both belonging to the Access group. Furthermore, of the total antibiotics prescribed, 41.9% were prescribed without adhering to the standard treatment guidelines. 
  Conclusion: This study found a high prescription of antibiotics (82.5%) that can be linked to non-adherence to the standard treatment guidelines in primary healthcare hospitals. The most prescribed antibiotic was ceftriaxone which belongs to the Watch group, raising a lot of concerns. There is a need for rational prescribing of antibiotics and implementation of AMS programs in healthcare facilities in Zambia, and this may promote surveillance of irrational prescribing and help reduce AMR in the future.
 
</p></abstract><kwd-group><kwd>Antibiotic Prescribing</kwd><kwd> Antimicrobial Resistance</kwd><kwd> Antimicrobial Stewardship</kwd><kwd> AWaRe Classification</kwd><kwd> Prescribing Patterns</kwd><kwd> Primary Healthcare</kwd><kwd> Surveillance</kwd><kwd> Zambia</kwd></kwd-group></article-meta></front><body><sec id="s1"><title>1. Introduction</title><p>Antibiotics have been critical in managing infectious diseases [<xref ref-type="bibr" rid="scirp.120529-ref1">1</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref2">2</xref>]. However, their inappropriate use has contributed to the development of antimicrobial resistance (AMR) [<xref ref-type="bibr" rid="scirp.120529-ref3">3</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref4">4</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref5">5</xref>]. AMR is a global public health issue that has been exacerbated by an increase in the consumption of antibiotics [<xref ref-type="bibr" rid="scirp.120529-ref3">3</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref4">4</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref6">6</xref>]. Prescribers of medicines may help reduce the problem of AMR by ensuring that they avoid overprescribing antibiotics [<xref ref-type="bibr" rid="scirp.120529-ref7">7</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref8">8</xref>]. Besides, they should adhere to the guidelines when prescribing antibiotics [<xref ref-type="bibr" rid="scirp.120529-ref8">8</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref9">9</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref10">10</xref>]. Additionally, all healthcare workers (HCWs) should collaborate to address AMR and promote antimicrobial stewardship (AMS) programs [<xref ref-type="bibr" rid="scirp.120529-ref11">11</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref12">12</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref13">13</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref14">14</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref15">15</xref>]. This can improve the surveillance and reduction of AMR [<xref ref-type="bibr" rid="scirp.120529-ref16">16</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref17">17</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref18">18</xref>].</p><p>The World Health Organization (WHO) developed the “Access”, “Watch”, and “Reserve” (AWaRe) classification of antibiotics to tackle AMR [<xref ref-type="bibr" rid="scirp.120529-ref19">19</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref20">20</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref21">21</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref22">22</xref>]. In the Access group, narrow-spectrum antibiotics are generally used as the first and second choice for most infections, while broad-spectrum antibiotics comprise the Watch group antibiotics [<xref ref-type="bibr" rid="scirp.120529-ref20">20</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref23">23</xref>]. Access group antibiotics must be readily available, affordable, and of good quality in treating infections [<xref ref-type="bibr" rid="scirp.120529-ref23">23</xref>]. The Reserve group contains last resort antibiotics and is usually used to treat multi-drug resistant infections [<xref ref-type="bibr" rid="scirp.120529-ref20">20</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref23">23</xref>]. Therefore, the reserve antibiotics must be left as a treatment of last resort, which may preserve the effectiveness of antibiotics [<xref ref-type="bibr" rid="scirp.120529-ref23">23</xref>]. Literature has shown that prescribers which adhere to the AWaRe protocol have reported a reduction in AMR cases in their healthcare facilities [<xref ref-type="bibr" rid="scirp.120529-ref24">24</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref25">25</xref>]. However, most prescribers do not adhere to the AWaRe protocol, thereby worsening the number of microorganisms developing resistance to antibiotics [<xref ref-type="bibr" rid="scirp.120529-ref26">26</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref27">27</xref>]. Conversely, in Ghana, prescribers adhered to the AWaRe classification protocol, indicating good AMS [<xref ref-type="bibr" rid="scirp.120529-ref28">28</xref>].</p><p>The AWaRe protocol of antibiotics is an important tool for AMS [<xref ref-type="bibr" rid="scirp.120529-ref29">29</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref30">30</xref>]. The tool may help prescribers minimise prescribing antibiotics and adhere to the prescription of less than 30% as recommended by the WHO [<xref ref-type="bibr" rid="scirp.120529-ref31">31</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref32">32</xref>]. The AWaRe protocol also guides prescribers to ensure that they prescribe more than 60% of Access group antibiotics compared to the other groups [<xref ref-type="bibr" rid="scirp.120529-ref33">33</xref>]. However, evidence has shown an overprescribing of Watch group antibiotics compared to Access antibiotics [<xref ref-type="bibr" rid="scirp.120529-ref27">27</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref30">30</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref33">33</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref34">34</xref>].</p><p>Evidence has shown that antibiotics are overprescribed in healthcare facilities across countries [<xref ref-type="bibr" rid="scirp.120529-ref26">26</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref35">35</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref36">36</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref37">37</xref>]. Approximately 20 to 50% of antibiotics are prescribed inappropriately without adhering to the standard treatment guidelines (STG) [<xref ref-type="bibr" rid="scirp.120529-ref33">33</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref35">35</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref38">38</xref>]. Therefore, educating prescribers about the rational prescribing of antibiotics is crucial to reducing AMR in the future [<xref ref-type="bibr" rid="scirp.120529-ref15">15</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref39">39</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref40">40</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref41">41</xref>]. Alongside, educating healthcare students about AMR is critical as they are the future HCWs [<xref ref-type="bibr" rid="scirp.120529-ref42">42</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref43">43</xref>].</p><p>In Zambia, AMR is of public health concern and has been reported in various studies [<xref ref-type="bibr" rid="scirp.120529-ref42">42</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref44">44</xref>] - [<xref ref-type="bibr" rid="scirp.120529-ref53">53</xref>]. However, little is known about the antibiotic prescribing patterns based on the WHO AWaRe classification in primary healthcare hospitals that offer primary healthcare services. Therefore, this study assessed antibiotic prescribing patterns in in-patients according to the WHO AWaRe classification in selected primary healthcare hospitals in Lusaka, Zambia.</p></sec><sec id="s2"><title>2. Materials and Methods</title><sec id="s2_1"><title>2.1. Study Design, Site and Population</title><p>This was a retrospective cross-sectional study that was conducted by reviewing medical records of in-patients in five first-level hospitals, namely Matero, Chawama, Chipata, Chilenje, and Kanyama in Lusaka, Zambia. In Zambia, first-level hospitals offer primary care services and usually act as the first point of contact with the healthcare system. The study was conducted from September 4<sup>th</sup> to November 9<sup>th</sup>, 2021, and we included all patient medical files from January 2021 to October 2021.</p></sec><sec id="s2_2"><title>2.2. Sample size Determination and Sampling Technique</title><p>The sample size was determined using the Raosoft online sample calculator [<xref ref-type="bibr" rid="scirp.120529-ref54">54</xref>]. With no known previous study done in primary healthcare hospitals in Zambia, a 50% prevalence was used at a 95% confidence level and a margin of error of 5%. This resulted in a sample size of 385 patient medical files. All patient medical files were randomly selected to increase the chance of every file being part of the study.</p></sec><sec id="s2_3"><title>2.3. Data Collection Tool</title><p>A data entry sheet was used to collect data on diseases diagnosed and antibiotics prescribed in primary healthcare hospitals in Lusaka, Zambia. Furthermore, a consent form was given to prescribers who agreed to participate in the study. The data collection tool was adapted from a similar study [<xref ref-type="bibr" rid="scirp.120529-ref55">55</xref>]. Before carrying out this study, a pilot survey was done using 30 patient medical files. Data collection was done by two data collectors who were trained on how to select patient medical files and data entry. The collected information included gender and age of the patient, name of the healthcare facility, antibiotic use, adherence to treatment guidelines, and type of antibiotics prescribed. Adherence to prescribing antibiotics was done based on the Zambia STG [<xref ref-type="bibr" rid="scirp.120529-ref56">56</xref>] and AWaRe classification was used to classify antibiotics into Access, Watch, and Reserve groups [<xref ref-type="bibr" rid="scirp.120529-ref22">22</xref>]. Overall, 388 patient medical files were selected and used in this study.</p></sec><sec id="s2_4"><title>2.4. Data Analysis</title><p>The collected data were entered into Microsoft Excel 2016 for cleaning and coding. Subsequently, the data was exported to the Statistical Package for Social Sciences (SPSS) for Windows Version 23 for analysis. Descriptive statistics were then presented in the form of tables.</p></sec></sec><sec id="s3"><title>3. Results</title><p>Of the 388 patient files that were screened, 52.3% were male, 19.3% were 34-41 years old, 82.5% (n = 320) received antibiotics, and 41.9% (n = 134) prescribers did not adhere to the STG as shown in <xref ref-type="table" rid="table1">Table 1</xref>.</p><p>The most prescribed antibiotic was ceftriaxone (20.3%) which belongs to the Watch group of antibiotics. However, the overall proportion showed that antibiotics belonging to the Access group were the most prescribed (55%) in primary healtcare hospitals. A total of 10 Access and 6 Watch antibiotics were prescribed (<xref ref-type="table" rid="table2">Table 2</xref>).</p></sec><sec id="s4"><title>4. Discussion</title><p>This study assessed antibiotic prescribing patterns in five primary healthcare hospitals in Lusaka, Zambia. The study reported a high rate (82.5%) of antibiotic prescribing, and ceftriaxone was the most prescribed for in-patients. Adherence to the national STG was found to be 58.1%, meaning that 41.9% of antibiotics were prescribed without adhering to the national STG.</p><p>The prevalence of antibiotic use in the present study was high. Our findings are in line with a study that was conducted in Iraq though a higher prevalence (93.7%) was reported [<xref ref-type="bibr" rid="scirp.120529-ref57">57</xref>], 88.2% in Eswatini [<xref ref-type="bibr" rid="scirp.120529-ref58">58</xref>], slightly lower prevalence (82.3%) in Pakistan [<xref ref-type="bibr" rid="scirp.120529-ref35">35</xref>], 74% in Uganda [<xref ref-type="bibr" rid="scirp.120529-ref59">59</xref>], and 60.6% in Ethiopia [<xref ref-type="bibr" rid="scirp.120529-ref60">60</xref>]. These findings are higher than the reference value of less than 30% recommended by the WHO [<xref ref-type="bibr" rid="scirp.120529-ref31">31</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref32">32</xref>]. This high use of antibiotics in healthcare facilities may be due to various diseases that in-patients suffer from and puts pressure on the prescribers to prescribe these drugs for disease prevention and treatment [<xref ref-type="bibr" rid="scirp.120529-ref61">61</xref>] but may promote the emergence of antibiotic-resistance microbes [<xref ref-type="bibr" rid="scirp.120529-ref62">62</xref>]. The</p><table-wrap id="table1" ><label><xref ref-type="table" rid="table1">Table 1</xref></label><caption><title> Sociodemographic characteristics</title></caption><table><tbody><thead><tr><th align="center" valign="middle" >Variable</th><th align="center" valign="middle" >Characteristic</th><th align="center" valign="middle" >Frequency (n = 388)</th><th align="center" valign="middle" >Percent (%)</th></tr></thead><tr><td align="center" valign="middle" >Gender</td><td align="center" valign="middle" >Female</td><td align="center" valign="middle" >185</td><td align="center" valign="middle" >47.7</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >Male</td><td align="center" valign="middle" >203</td><td align="center" valign="middle" >52.3</td></tr><tr><td align="center" valign="middle" >Age (years)</td><td align="center" valign="middle" >18 - 25</td><td align="center" valign="middle" >72</td><td align="center" valign="middle" >18.6</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >26 - 33</td><td align="center" valign="middle" >64</td><td align="center" valign="middle" >16.5</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >34 - 41</td><td align="center" valign="middle" >75</td><td align="center" valign="middle" >19.3</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >42 - 49</td><td align="center" valign="middle" >60</td><td align="center" valign="middle" >15.5</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >50 - 57</td><td align="center" valign="middle" >39</td><td align="center" valign="middle" >10.1</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >58 - 65</td><td align="center" valign="middle" >29</td><td align="center" valign="middle" >7.5</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >&gt;65</td><td align="center" valign="middle" >49</td><td align="center" valign="middle" >12.6</td></tr><tr><td align="center" valign="middle" >Healthcare facility</td><td align="center" valign="middle" >Chawama</td><td align="center" valign="middle" >78</td><td align="center" valign="middle" >20.1</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >Chilenje</td><td align="center" valign="middle" >67</td><td align="center" valign="middle" >17.3</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >Chipata</td><td align="center" valign="middle" >72</td><td align="center" valign="middle" >18.6</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >Kanyama</td><td align="center" valign="middle" >87</td><td align="center" valign="middle" >22.4</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >Matero</td><td align="center" valign="middle" >84</td><td align="center" valign="middle" >21.6</td></tr><tr><td align="center" valign="middle" >Antibiotic use</td><td align="center" valign="middle" >No</td><td align="center" valign="middle" >68</td><td align="center" valign="middle" >17.5</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >Yes</td><td align="center" valign="middle" >320</td><td align="center" valign="middle" >82.5</td></tr><tr><td align="center" valign="middle" >Adherence to STG</td><td align="center" valign="middle" >No</td><td align="center" valign="middle" >134</td><td align="center" valign="middle" >41.9</td></tr><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" >Yes</td><td align="center" valign="middle" >186</td><td align="center" valign="middle" >58.1</td></tr></tbody></table></table-wrap><table-wrap id="table2" ><label><xref ref-type="table" rid="table2">Table 2</xref></label><caption><title> Prescribing patterns of antibiotics according to WHO AWaRe classification</title></caption><table><tbody><thead><tr><th align="center" valign="middle" >Antibiotic name</th><th align="center" valign="middle" >Access, n (%)</th><th align="center" valign="middle" >Watch, n (%)</th></tr></thead><tr><td align="center" valign="middle" >Amoxicillin</td><td align="center" valign="middle" >8 (2.5)</td><td align="center" valign="middle" >-</td></tr><tr><td align="center" valign="middle" >Amoxicillin/clavulanic acid</td><td align="center" valign="middle" >3 (0.9)</td><td align="center" valign="middle" >-</td></tr><tr><td align="center" valign="middle" >Azithromycin</td><td align="center" valign="middle" >-</td><td align="center" valign="middle" >37 (11.6)</td></tr><tr><td align="center" valign="middle" >Cefotaxime</td><td align="center" valign="middle" >-</td><td align="center" valign="middle" >8 (2.5)</td></tr><tr><td align="center" valign="middle" >Ceftriaxone</td><td align="center" valign="middle" >-</td><td align="center" valign="middle" >65 (20.3)</td></tr><tr><td align="center" valign="middle" >Cefuroxime</td><td align="center" valign="middle" >-</td><td align="center" valign="middle" >2 (0.6)</td></tr><tr><td align="center" valign="middle" >Cephalexin</td><td align="center" valign="middle" >4 (1.3)</td><td align="center" valign="middle" >-</td></tr><tr><td align="center" valign="middle" >Chloramphenicol</td><td align="center" valign="middle" >2 (0.6)</td><td align="center" valign="middle" >-</td></tr><tr><td align="center" valign="middle" >Ciprofloxacin</td><td align="center" valign="middle" >-</td><td align="center" valign="middle" >31 (9.7)</td></tr><tr><td align="center" valign="middle" >Cloxacillin</td><td align="center" valign="middle" >27 (8.4)</td><td align="center" valign="middle" >-</td></tr><tr><td align="center" valign="middle" >Doxycycline</td><td align="center" valign="middle" >5 (1.6)</td><td align="center" valign="middle" >-</td></tr><tr><td align="center" valign="middle" >Erythromycin</td><td align="center" valign="middle" >-</td><td align="center" valign="middle" >2 (0.6)</td></tr><tr><td align="center" valign="middle" >Gentamicin</td><td align="center" valign="middle" >15 (4.7)</td><td align="center" valign="middle" >-</td></tr><tr><td align="center" valign="middle" >Metronidazole</td><td align="center" valign="middle" >57 (17.8)</td><td align="center" valign="middle" >-</td></tr><tr><td align="center" valign="middle" >Phenoxymethylpenicillin</td><td align="center" valign="middle" >2 (0.6)</td><td align="center" valign="middle" >-</td></tr><tr><td align="center" valign="middle" >Sulfamethoxazole/trimethoprim</td><td align="center" valign="middle" >52 (16.3)</td><td align="center" valign="middle" >-</td></tr><tr><td align="center" valign="middle" >Total</td><td align="center" valign="middle" >175 (55)</td><td align="center" valign="middle" >145 (45)</td></tr></tbody></table></table-wrap><p>most prescribed antibiotic in our study was ceftriaxone (20.3%) which belongs to the Watch group. These findings are comparable with reports from other countries [<xref ref-type="bibr" rid="scirp.120529-ref33">33</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref35">35</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref59">59</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref60">60</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref63">63</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref64">64</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref65">65</xref>]. The high prescription rate of ceftriaxone has a high resistance potential and should not be prescribed routinely [<xref ref-type="bibr" rid="scirp.120529-ref65">65</xref>]. The over-prescription and use of ceftriaxone also highlight the need for antibiotic prescription guidelines at these facilities per national and international guidelines to reduce its irrational use. Contrary to our findings, the most prescribed antibiotic was amoxicillin in Eswatini [<xref ref-type="bibr" rid="scirp.120529-ref58">58</xref>], penicillins in China due to increased respiratory tract infections [<xref ref-type="bibr" rid="scirp.120529-ref62">62</xref>], and metronidazole in Ghana due to increased dental and gastrointestinal problems [<xref ref-type="bibr" rid="scirp.120529-ref28">28</xref>].</p><p>Our study revealed that most prescribed antibiotics belonged to the Access group. These findings corroborate reports from a point prevalence survey across six hospitals in Tanzania that revealed that most patients received antibiotics from the Access group [<xref ref-type="bibr" rid="scirp.120529-ref66">66</xref>], similar to what was reported in Eswatini [<xref ref-type="bibr" rid="scirp.120529-ref58">58</xref>], Ghana [<xref ref-type="bibr" rid="scirp.120529-ref28">28</xref>], and Uganda [<xref ref-type="bibr" rid="scirp.120529-ref59">59</xref>]. On the contrary, In China, a study revealed that most antibiotics consumed in healthcare facilities belonged to the Watch group [<xref ref-type="bibr" rid="scirp.120529-ref67">67</xref>]. According to a point prevalence survey carried out in 69 countries, the research found that the overall use of Watch group antibiotics was high, and stratification by World Bank classification showed that hospitals in lower-middle- and upper-middle-income countries contributed substantially to the proportion of Watch antibiotics [<xref ref-type="bibr" rid="scirp.120529-ref30">30</xref>]. Worldwide, a large proportion of Reserve group antibiotics were prescribed empirically [<xref ref-type="bibr" rid="scirp.120529-ref30">30</xref>]. In lower-middle-income countries, up to 53.0% of all Reserve prescriptions were empirical, which indicates a lack of diagnostic capacity [<xref ref-type="bibr" rid="scirp.120529-ref30">30</xref>]. This indicated poor prescribing patterns in these facilities and calls for strict implementation of AMS programs.</p><p>Interestingly, our study found that 55% of Access, 45% of Watch and no Reserve group antibiotics were prescribed. Unfortunately, this is not in line with the WHO recommendations in which Access group antibiotics must be prescribed more than 60% of all antibiotic prescriptions [<xref ref-type="bibr" rid="scirp.120529-ref33">33</xref>]. In Uganda, similarly, despite the Access group antibiotics reported to be prescribed more than Watch group antibiotics, the proportion was 47.2%, which did not meet the WHO recommendations [<xref ref-type="bibr" rid="scirp.120529-ref59">59</xref>]. In India, a study reported that 42.3% of Access group antibiotics were prescribed with no Reserve antibiotics recorded in their findings [<xref ref-type="bibr" rid="scirp.120529-ref63">63</xref>]. Since these findings did not meet the WHO recommendations of AWaRe prescribing of antibiotics, this may mean non-adherence to the protocols and a contributing factor to AMR in most healthcare facilities. In many health settings, non-adherence to protocols has been attributed to prescriber preferences [<xref ref-type="bibr" rid="scirp.120529-ref59">59</xref>], which may be the case in the current study. This result highlights the need for urgent AMS in these facilities, as prescribing watch antibiotics may scale up AMR and lead to the prescription of Reserve antibiotics. In contrast to our findings, other surveys reported the use of Access group antibiotics as more than 60% as recommended by the WHO [<xref ref-type="bibr" rid="scirp.120529-ref58">58</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref64">64</xref>]. Similar to our study finding regarding Reserve group antibiotics, other studies also found that no Reserve group antibiotics were prescribed in their surveys [<xref ref-type="bibr" rid="scirp.120529-ref58">58</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref63">63</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref68">68</xref>]. This is a positive finding because Reserve group antibiotics must be preserved as the last resort of treatment after other options have failed. To maintain the status quo, AMS programs must be implemented or enhanced.</p><p>Of note is that some prescribers in our study did not adhere to the treatment guidelines. This practice is inappropriate and may contribute to the development of AMR. Similar findings were reported in other surveys where the overall compliance with the outlined prescribing guidelines was suboptimal [<xref ref-type="bibr" rid="scirp.120529-ref57">57</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref69">69</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref70">70</xref>]. Lower adherence to treatment guidelines was reported in Uganda [<xref ref-type="bibr" rid="scirp.120529-ref59">59</xref>]. Non-adherence to the standard treatment guidelines of infectious diseases may be due to the absence of these guidelines in healthcare facilities [<xref ref-type="bibr" rid="scirp.120529-ref35">35</xref>] [<xref ref-type="bibr" rid="scirp.120529-ref59">59</xref>], out of stock of key antibiotics [<xref ref-type="bibr" rid="scirp.120529-ref60">60</xref>], prescriber preferences, lack of efficient laboratory services and lack of proper diagnostic stewardship [<xref ref-type="bibr" rid="scirp.120529-ref59">59</xref>]. Additionally, shortages of medicines, increased burden of disease, and lack of healthcare workers put pressure on the prescribers leading to non-adherence to STGs when prescribing [<xref ref-type="bibr" rid="scirp.120529-ref71">71</xref>].</p><p>The current study findings may help identify key areas that require interventions through the promotion of AMS programs across healthcare facilities in Zambia. The study also highlights the need for rational prescribing and adherence to the National STG. Additionally, this calls for sensitisation and educational activities on the rational use of antibiotics across healthcare workers. Ministries responsible for health must ensure that all antibiotics listed under the Essential Medicines List (EML) are available to avoid inflicting pressure on prescribers and overuse of Watch group antibiotics.</p><p>This study was conducted in one province of Zambia, hence, the findings may not be generalized to the other provinces across the country.</p></sec><sec id="s5"><title>5. Conclusion</title><p>Our study found high prescribing of antibiotics without adhering to the National Treatment Guidelines by the prescribers. Ceftriaxone, a Watch group antibiotic, was the most prescribed medicine, and this requires prescriber educational and training activities on the AWaRe protocol and adherence to the treatment guidelines. Therefore, AMS programs should be implemented and enhanced across healthcare facilities in Zambia.</p></sec><sec id="s6"><title>Ethical Approval</title><p>This study was approved by the University of Zambia Health Sciences Research Ethics Committee (UNZAHSREC) with protocol ID 202112030048.</p></sec><sec id="s7"><title>Acknowledgements</title><p>We are grateful to the management of the primary healthcare facilities that allowed us to collect the data we used in this study.</p></sec><sec id="s8"><title>Conflicts of Interest</title><p>The authors declare no conflicts of interest regarding the publication of this paper.</p></sec><sec id="s9"><title>Cite this paper</title><p>Mudenda, S., Chomba, M., Chabalenge, B., Hikaambo, C.N., Banda, M., Daka, V., Zulu, A., Mukesela, A., Kasonde, M., Lukonde, P., Chikatula, E., Matowe, L., Mutati, R.K., Muungo, T.L., Mudenda, T., Mohamed, S. and Matafwali, S. (2022) Antibiotic Prescribing Patterns in Adult Patients According to the WHO AWaRe Classification: A Multi-Facility Cross-Sectional Study in Primary Healthcare Hospitals in Lusaka, Zambia. Pharmacology &amp; Pharmacy, 13, 379-392. https://doi.org/10.4236/pp.2022.1310029</p></sec></body><back><ref-list><title>References</title><ref id="scirp.120529-ref1"><label>1</label><mixed-citation publication-type="journal" xlink:type="simple"><name name-style="western"><surname>Adedeji</surname><given-names> W.A. </given-names></name>,<etal>et al</etal>. (<year>2016</year>)<article-title>The Treasure Called Antibiotics</article-title><source> Annals of Ibadan Postgraduate Medicine</source><volume> 14</volume>,<fpage> 56</fpage>-<lpage>57</lpage>.<pub-id pub-id-type="doi"></pub-id></mixed-citation></ref><ref id="scirp.120529-ref2"><label>2</label><mixed-citation publication-type="other" xlink:type="simple">Nigam, A., Gupta, D. and Sharma, A. (2014) Treatment of Infectious Disease: Beyond Antibiotics. Microbiological Research, 169, 643-651.  
https://doi.org/10.1016/j.micres.2014.02.009</mixed-citation></ref><ref id="scirp.120529-ref3"><label>3</label><mixed-citation publication-type="other" xlink:type="simple">Ramachandran, P., Rachuri, N., Martha, S., Shakthivel, R., Gundala, A. and Battu, T. (2019) Implications of Overprescription of Antibiotics: A Cross-Sectional Study. Journal of Pharmacy &amp; Bioallied Sciences, 11, 434-437.  
https://www.jpbsonline.org/article.asp?issn=0975-7406;year=2019;volume=11;issue=6;spage=434;epage=437;aulast=Ramachandran   
https://doi.org/10.4103/JPBS.JPBS_62_19</mixed-citation></ref><ref id="scirp.120529-ref4"><label>4</label><mixed-citation publication-type="other" xlink:type="simple">Llor, C. and Bjerrum, L. (2014) Antimicrobial Resistance: Risk Associated with Antibiotic Overuse and Initiatives to Reduce the Problem. Therapeutic Advances in Drug Safety, 5, 229-241.  
https://journals.sagepub.com/doi/10.1177/2042098614554919   
https://doi.org/10.1177/2042098614554919</mixed-citation></ref><ref id="scirp.120529-ref5"><label>5</label><mixed-citation publication-type="other" xlink:type="simple">Belachew, S.A., Hall, L. and Selvey, L.A. (2022) Community Drug Retail Outlet Staff’s Knowledge, Attitudes and Practices towards Non-Prescription Antibiotics Use and Antibiotic Resistance in the Amhara Region, Ethiopia with a Focus on Non-Urban Towns. Antimicrobial Resistance &amp; Infection Control, 11, Article No. 64. https://aricjournal.biomedcentral.com/articles/10.1186/s13756-022-01102-1   
https://doi.org/10.1186/s13756-022-01102-1</mixed-citation></ref><ref id="scirp.120529-ref6"><label>6</label><mixed-citation publication-type="other" xlink:type="simple">Saliba-Gustafsson, E.A., Nyberg, A., Borg, M.A., Rosales-Klintz, S. and Lundborg, C.S. (2021) Barriers and Facilitators to Prudent Antibiotic Prescribing for Acute Respiratory Tract Infections: A Qualitative Study with General Practitioners in Malta. PLOS ONE, 16, e0246782.  
https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0246782   
https://doi.org/10.1371/journal.pone.0246782</mixed-citation></ref><ref id="scirp.120529-ref7"><label>7</label><mixed-citation publication-type="other" xlink:type="simple">Wilkinson, A., Ebata, A. and Macgregor, H. (2019) Interventions to Reduce Antibiotic Prescribing in LMICs: A Scoping Review of Evidence from Human and Animal Health Systems. Antibiotics, 8, Article 2.  
https://www.mdpi.com/2079-6382/8/1/2/htm   
https://doi.org/10.3390/antibiotics8010002</mixed-citation></ref><ref id="scirp.120529-ref8"><label>8</label><mixed-citation publication-type="other" xlink:type="simple">McDonagh, M.S., Peterson, K., Winthrop, K., Cantor, A., Lazur, B.H. and Buckley, D.I. (2018) Interventions to Reduce Inappropriate Prescribing of Antibiotics for Acute Respiratory Tract Infections: Summary and Update of a Systematic Review. Journal of International Medical Research, 46, S3337-S3357.  
https://doi.org/10.1177/0300060518782519</mixed-citation></ref><ref id="scirp.120529-ref9"><label>9</label><mixed-citation publication-type="other" xlink:type="simple">Oliveira, I., Rego, C., Semedo, G., Gomes, D., Figueiras, A., Roque, F., et al. (2020) Systematic Review on the Impact of Guidelines Adherence on Antibiotic Prescription in Respiratory Infections. Antibiotics, 9, Article 546.  
https://doi.org/10.3390/antibiotics9090546</mixed-citation></ref><ref id="scirp.120529-ref10"><label>10</label><mixed-citation publication-type="other" xlink:type="simple">Tell, D., Engstrom, S. and Molstad, S. (2015) Adherence to Guidelines on Antibiotic Treatment for Respiratory Tract Infections in Various Categories of Physicians: A Retrospective Cross-Sectional Study of Data from Electronic Patient Records. BMJ Open, 5, e008096. https://bmjopen.bmj.com/content/5/7/e008096   
https://doi.org/10.1136/bmjopen-2015-008096</mixed-citation></ref><ref id="scirp.120529-ref11"><label>11</label><mixed-citation publication-type="other" xlink:type="simple">McKenzie, D., Rawlins, M. and Del Mar, C. (2013) Antimicrobial Stewardship: What’s It All about? Australian Prescriber, 36, 116-120.  
https://www.nps.org.au/australian-prescriber/articles/antimicrobial-stewardship-whats-it-all-about</mixed-citation></ref><ref id="scirp.120529-ref12"><label>12</label><mixed-citation publication-type="other" xlink:type="simple">Kimbowa, I.M., Eriksen, J., Nakafeero, M., Obua, C., Lundborg, C.S., Kalyango, J., et al. (2022) Antimicrobial Stewardship: Attitudes and Practices of Healthcare Providers in Selected Health Facilities in Uganda. PLOS ONE, 17, e0262993.  
https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0262993  
https://doi.org/10.1371/journal.pone.0262993</mixed-citation></ref><ref id="scirp.120529-ref13"><label>13</label><mixed-citation publication-type="other" xlink:type="simple">Doornebosch, A.J., Smaling, H.J.A. and Achterberg, W.P. (2022) Interprofessional Collaboration in Long-Term Care and Rehabilitation: A Systematic Review. Journal of the American Medical Directors Association, 23, 764-777.e2.  
https://doi.org/10.1016/j.jamda.2021.12.028</mixed-citation></ref><ref id="scirp.120529-ref14"><label>14</label><mixed-citation publication-type="other" xlink:type="simple">Rogers Van Katwyk, S., Jones, S.L. and Hoffman, S.J. (2018) Mapping Educational Opportunities for Healthcare Workers on Antimicrobial Resistance and Stewardship around the World. Human Resources for Health, 16, Article No. 9.  
https://human-resources-health.biomedcentral.com/articles/10.1186/s12960-018-0270-3   
https://doi.org/10.1186/s12960-018-0270-3</mixed-citation></ref><ref id="scirp.120529-ref15"><label>15</label><mixed-citation publication-type="other" xlink:type="simple">Godman, B., Egwuenu, A., Haque, M., Malande, O.O., Schellack, N., Kumar, S., et al. (2021) Strategies to Improve Antimicrobial Utilization with a Special Focus on Developing Countries. Life, 11, Article 528.  
https://pubmed.ncbi.nlm.nih.gov/34200116/   
https://doi.org/10.3390/life11060528</mixed-citation></ref><ref id="scirp.120529-ref16"><label>16</label><mixed-citation publication-type="other" xlink:type="simple">Tacconelli, E., Sifakis, F., Harbarth, S., Schrijver, R., van Mourik, M., Voss, A., et al. (2018) Surveillance for Control of Antimicrobial Resistance. The Lancet Infectious Diseases, 18, e99-e106. https://doi.org/10.1016/S1473-3099(17)30485-1</mixed-citation></ref><ref id="scirp.120529-ref17"><label>17</label><mixed-citation publication-type="other" xlink:type="simple">Johnson, A.P., Muller-Pebody, B., Budd, E., Ashiru-Oredope, D., Ladenheim, D., Hain, D., et al. (2017) Improving Feedback of Surveillance Data on Antimicrobial Consumption, Resistance and Stewardship in England: Putting the Data at Your Fingertips. Journal of Antimicrobial Chemotherapy, 72, 953-956.  
https://doi.org/10.1093/jac/dkw536</mixed-citation></ref><ref id="scirp.120529-ref18"><label>18</label><mixed-citation publication-type="other" xlink:type="simple">Fadare, J.O., Ogunleye, O., Iliyasu, G., Adeoti, A., Schellack, N., Engler, D., et al. (2019) Status of Antimicrobial Stewardship Programmes in Nigerian Tertiary Healthcare Facilities: Findings and Implications. Journal of Global Antimicrobial Resistance, 17, 132-136. https://doi.org/10.1016/j.jgar.2018.11.025</mixed-citation></ref><ref id="scirp.120529-ref19"><label>19</label><mixed-citation publication-type="other" xlink:type="simple">Budd, E., Cramp, E., Sharland, M., Hand, K., Howard, P., Wilson, P., et al. (2019) Adaptation of the WHO Essential Medicines List for National Antibiotic Stewardship Policy in England: Being AWaRe. Journal of Antimicrobial Chemotherapy, 74, 3384-3389. https://doi.org/10.1093/jac/dkz321</mixed-citation></ref><ref id="scirp.120529-ref20"><label>20</label><mixed-citation publication-type="other" xlink:type="simple">Hsia, Y., Lee, B.R., Versporten, A., Yang, Y., Bielicki, J., Jackson, C., et al. (2019) Use of the WHO Access, Watch, and Reserve Classification to Define Patterns of Hospital Antibiotic Use (AWaRe): An Analysis of Paediatric Survey Data from 56 Countries. The Lancet Global Health, 7, e861-e871. https://www.global-pps.com</mixed-citation></ref><ref id="scirp.120529-ref21"><label>21</label><mixed-citation publication-type="other" xlink:type="simple">Sharland, M., Pulcini, C., Harbarth, S., Zeng, M., Gandra, S., Mathur, S., et al. (2018) Classifying Antibiotics in the WHO Essential Medicines List for Optimal Use—Be AWaRe. The Lancet Infectious Diseases, 18, 18-20.  
https://doi.org/10.1016/S1473-3099(17)30724-7</mixed-citation></ref><ref id="scirp.120529-ref22"><label>22</label><mixed-citation publication-type="other" xlink:type="simple">World Health Organization (2021) 2021 AWaRe Classification. WHO.  
https://www.who.int/publications/i/item/2021-aware-classification</mixed-citation></ref><ref id="scirp.120529-ref23"><label>23</label><mixed-citation publication-type="other" xlink:type="simple">McGettigan, P., Roderick, P., Kadam, A. and Pollock, A.M. (2017) Access, Watch, and Reserve Antibiotics in India: Challenges for WHO Stewardship. The Lancet Global Health, 5, e1075-e1076. https://doi.org/10.1016/S2214-109X(17)30365-0</mixed-citation></ref><ref id="scirp.120529-ref24"><label>24</label><mixed-citation publication-type="other" xlink:type="simple">Majumder, M.A.A., Rahman, S., Cohall, D., Bharatha, A., Singh, K., Haque, M., et al. (2020) Antimicrobial Stewardship: Fighting Antimicrobial Resistance and Protecting Global Public Health. Infection and Drug Resistance, 13, 4713-4738.  
https://doi.org/10.2147/IDR.S290835</mixed-citation></ref><ref id="scirp.120529-ref25"><label>25</label><mixed-citation publication-type="other" xlink:type="simple">Sulis, G., Sayood, S., Katukoori, S., Bollam, N., George, I., Yaeger, L.H., et al. (2022) Exposure to World Health Organization’s AWaRe Antibiotics and Isolation of Multi-Drug Resistant Bacteria: A Systematic Review and Meta-Analysis. Clinical Microbiology and Infection, 28, 1193-1202.  
https://doi.org/10.1016/j.cmi.2022.03.014</mixed-citation></ref><ref id="scirp.120529-ref26"><label>26</label><mixed-citation publication-type="other" xlink:type="simple">Amaha, N.D., Weldemariam, D.G., Abdu, N. and Tesfamariam, E.H. (2019) Prescribing Practices Using WHO Prescribing Indicators and Factors Associated with Antibiotic Prescribing in Six Community Pharmacies in Asmara, Eritrea: A Cross-Sectional Study. Antimicrobial Resistance &amp; Infection Control, 8, Article No. 163. https://aricjournal.biomedcentral.com/articles/10.1186/s13756-019-0620-5  
https://doi.org/10.1186/s13756-019-0620-5</mixed-citation></ref><ref id="scirp.120529-ref27"><label>27</label><mixed-citation publication-type="other" xlink:type="simple">Thomas, A.P., Kumar, M., Johnson, R., More, S.P. and Panda, B.K. (2022) Evaluation of Antibiotic Consumption and Compliance to Hospital Antibiotic Policy in the Surgery, Orthopedics and Gynecology Wards of a Tertiary Care Hospital. Clinical Epidemiology and Global Health, 13, Article ID: 100944.  
https://doi.org/10.1016/j.cegh.2021.100944</mixed-citation></ref><ref id="scirp.120529-ref28"><label>28</label><mixed-citation publication-type="other" xlink:type="simple">Darkwah, T.O., Afriyie, D.K., Sneddon, J., Cockburn, A., Opare-Addo, M.N.A., Tagoe, B., et al. (2021) Assessment of Prescribing Patterns of Antibiotics Using National Treatment Guidelines and World Health Organization Prescribing Indicators at the Ghana Police Hospital: A Pilot Study. The Pan African Medical Journal, 39, Article 222. https://www.panafrican-med-journal.com/content/article/39/222/full  
https://doi.org/10.11604/pamj.2021.39.222.29569</mixed-citation></ref><ref id="scirp.120529-ref29"><label>29</label><mixed-citation publication-type="other" xlink:type="simple">Hillock, N.T., Connor, E., Wilson, C. and Kennedy, B. (2021) Comparative Analysis of Australian Hospital Antimicrobial Utilization, Using the WHO AWaRe Classification System and the Adapted Australian Priority Antimicrobial List (PAL). JAC-Antimicrobial Resistance, 3, dlab017. https://doi.org/10.1093/jacamr/dlab017</mixed-citation></ref><ref id="scirp.120529-ref30"><label>30</label><mixed-citation publication-type="other" xlink:type="simple">Pauwels, I., Versporten, A., Drapier, N., Vlieghe, E. and Goossens, H. (2021) Hospital Antibiotic Prescribing Patterns in Adult Patients According to the WHO Access, Watch and Reserve Classification (AWaRe): Results from a Worldwide Point Prevalence Survey in 69 Countries. Journal of Antimicrobial Chemotherapy, 76, 1614-1624.  
https://academic.oup.com/jac/article/76/6/1614/6210595  
https://doi.org/10.1093/jac/dkab050</mixed-citation></ref><ref id="scirp.120529-ref31"><label>31</label><mixed-citation publication-type="other" xlink:type="simple">Ofori-Asenso, R., Brhlikova, P. and Pollock, A.M. (2016) Prescribing Indicators at Primary Health Care Centers within the WHO African Region: A Systematic Analysis (1995-2015). BMC Public Health, 16, Article No. 724.  
https://bmcpublichealth.biomedcentral.com/articles/10.1186/s12889-016-3428-8   
https://doi.org/10.1186/s12889-016-3428-8</mixed-citation></ref><ref id="scirp.120529-ref32"><label>32</label><mixed-citation publication-type="other" xlink:type="simple">Ofori-Asenso, R. (2016) A Closer Look at the World Health Organization’s Prescribing Indicators. Journal of Pharmacology and Pharmacotherapeutics, 7, 51-54.  
http://www.ncbi.nlm.nih.gov/pubmed/27127400   
https://doi.org/10.4103/0976-500X.179352</mixed-citation></ref><ref id="scirp.120529-ref33"><label>33</label><mixed-citation publication-type="other" xlink:type="simple">Mugada, V., Mahato, V., Andhavaram, D. and Vajhala, S.M. (2021) Evaluation of Prescribing Patterns of Antibiotics Using Selected Indicators for Antimicrobial Use in Hospitals and the Access, Watch, Reserve (AWaRe) Classification by the World Health Organization. Turkish Journal of Pharmaceutical Sciences 18, 282-288.  
https://pubmed.ncbi.nlm.nih.gov/34157817/   
https://doi.org/10.4274/tjps.galenos.2020.11456</mixed-citation></ref><ref id="scirp.120529-ref34"><label>34</label><mixed-citation publication-type="other" xlink:type="simple">Zhussupova, G., Utepova, D., Orazova, G., Zhaldybayeva, S., Skvirskaya, G. and Tossekbayev, K. (2021) Evaluation of Antibiotic Use in Kazakhstan for the Period 2017-2019 Based on Who Access, Watch and Reserve Classification (AWaRe 2019). Antibiotics, 10, Article 58. https://www.mdpi.com/2079-6382/10/1/58/htm   
https://doi.org/10.3390/antibiotics10010058</mixed-citation></ref><ref id="scirp.120529-ref35"><label>35</label><mixed-citation publication-type="other" xlink:type="simple">Atif, M., Azeem, M., Saqib, A. and Scahill, S. (2017) Investigation of Antimicrobial Use at a Tertiary Care Hospital in Southern Punjab, Pakistan Using WHO Methodology. Antimicrobial Resistance &amp; Infection Control, 6, Article No. 41.  
https://aricjournal.biomedcentral.com/articles/10.1186/s13756-017-0199-7   
https://doi.org/10.1186/s13756-017-0199-7</mixed-citation></ref><ref id="scirp.120529-ref36"><label>36</label><mixed-citation publication-type="other" xlink:type="simple">Sulis, G., Daniels, B., Kwan, A., Gandra, S., Daftary, A., Das, J., et al. (2020) Antibiotic Overuse in the Primary Health Care Setting: A Secondary Data Analysis of Standardised Patient Studies from India, China and Kenya. BMJ Global Health, 5, e003393. https://gh.bmj.com/content/5/9/e003393   
https://doi.org/10.1136/bmjgh-2020-003393</mixed-citation></ref><ref id="scirp.120529-ref37"><label>37</label><mixed-citation publication-type="other" xlink:type="simple">O’Doherty, J., Leader, L.F.W., O’Regan, A., Dunne, C., Puthoopparambil, S.J. and O’Connor, R. (2019) Over Prescribing of Antibiotics for Acute Respiratory Tract Infections; A Qualitative Study to Explore Irish General Practitioners’ Perspectives. BMC Family Practice, 20, Article No. 27.  
https://bmcprimcare.biomedcentral.com/articles/10.1186/s12875-019-0917-8   
https://doi.org/10.1186/s12875-019-0917-8</mixed-citation></ref><ref id="scirp.120529-ref38"><label>38</label><mixed-citation publication-type="other" xlink:type="simple">Andrajati, R., Tilaqza, A. and Supardi, S. (2017) Factors Related to Rational Antibiotic Prescriptions in Community Health Centers in Depok City, Indonesia. Journal of Infection and Public Health, 10, 41-48. https://doi.org/10.1016/j.jiph.2016.01.012</mixed-citation></ref><ref id="scirp.120529-ref39"><label>39</label><mixed-citation publication-type="other" xlink:type="simple">Jiang, T.T., Yang, Y.Q., Cao, N.X., Yin, Y.P. and Chen, X.S. (2020) Novel Education-Based Intervention to Reduce Inappropriate Antibiotic Prescribing for Treatment of Gonorrhoea in China: Protocol for a Cluster Randomised Controlled Trial. BMJ Open, 10, e037549. https://bmjopen.bmj.com/content/10/7/e037549   
https://doi.org/10.1136/bmjopen-2020-037549</mixed-citation></ref><ref id="scirp.120529-ref40"><label>40</label><mixed-citation publication-type="other" xlink:type="simple">Ozcebe, H., üner, S., Karadag, O., Daryani, A., Gershuni, O., Czabanowska, K., et al. (2022) Perspectives of Physicians and Pharmacists on Rational Use of Antibiotics in Turkey and among Turkish Migrants in Germany, Sweden and the Netherlands: A Qualitative Study. BMC Primary Care, 23, Article No. 29.  
https://bmcprimcare.biomedcentral.com/articles/10.1186/s12875-022-01636-8   
https://doi.org/10.1186/s12875-022-01636-8</mixed-citation></ref><ref id="scirp.120529-ref41"><label>41</label><mixed-citation publication-type="other" xlink:type="simple">de With, K., Allerberger, F., Amann, S., Apfalter, P., Brodt, H.R., Eckmanns, T., et al. (2016) Strategies to Enhance Rational Use of Antibiotics in Hospital: A Guideline by the German Society for Infectious Diseases. Infection, 44, 395-439.  
https://link.springer.com/article/10.1007/s15010-016-0885-z   
https://doi.org/10.1007/s15010-016-0885-z</mixed-citation></ref><ref id="scirp.120529-ref42"><label>42</label><mixed-citation publication-type="other" xlink:type="simple">Mudenda, S., Mukela, M., Matafwali, S., Banda, M., Mutati, R.K., Muungo, L.T., et al. (2022) Knowledge, Attitudes, and Practices towards Antibiotic Use and Antimicrobial Resistance among Pharmacy Students at the University of Zambia: Implications for Antimicrobial Stewardship Programmes. Scholars Academic Journal of Pharmacy, 11, 117-124. https://doi.org/10.36347/sajp.2022.v11i08.002</mixed-citation></ref><ref id="scirp.120529-ref43"><label>43</label><mixed-citation publication-type="other" xlink:type="simple">Efthymiou, P., Gkentzi, D. and Dimitriou, G. (2020) Knowledge, Attitudes and Perceptions of Medical Students on Antimicrobial Stewardship. Antibiotics, 9, Article 821. https://doi.org/10.3390/antibiotics9110821</mixed-citation></ref><ref id="scirp.120529-ref44"><label>44</label><mixed-citation publication-type="other" xlink:type="simple">Mudenda, S., Malama, S., Munyeme, M., Hang’ombe, B.M., Mainda, G., Kapona, O., et al. (2022) Awareness of Antimicrobial Resistance and Associated Factors among Layer Poultry Farmers in Zambia: Implications for Surveillance and Antimicrobial Stewardship Programs. Antibiotics, 11, Article 383.  
https://pubmed.ncbi.nlm.nih.gov/35326846/   
https://doi.org/10.3390/antibiotics11030383</mixed-citation></ref><ref id="scirp.120529-ref45"><label>45</label><mixed-citation publication-type="other" xlink:type="simple">Mudenda, S., Mukosha, M., Godman, B., Fadare, J., Malama, S., Munyeme, M., et al. (2022) Knowledge, Attitudes and Practices of Community Pharmacy Professionals on Poultry Antimicrobial Dispensing, Use and Resistance in Zambia: Implications on Antibiotic Stewardship and WHO AWaRe Classification of Antibiotics. Antibiotics, 11, Article 1210. https://www.mdpi.com/2079-6382/11/9/1210/htm   
https://doi.org/10.3390/antibiotics11091210</mixed-citation></ref><ref id="scirp.120529-ref46"><label>46</label><mixed-citation publication-type="other" xlink:type="simple">Mpundu, P., Muma, J.B., Mukubesa, A.N., Kainga, H., Mudenda, S., Bumbangi, F.N., et al. (2022) Antibiotic Resistance Patterns of Listeria Species Isolated from Broiler Abattoirs in Lusaka, Zambia. Antibiotics, 11, Article 591.  
https://www.mdpi.com/2079-6382/11/5/591/htm   
https://doi.org/10.3390/antibiotics11050591</mixed-citation></ref><ref id="scirp.120529-ref47"><label>47</label><mixed-citation publication-type="other" xlink:type="simple">Samutela, M.T., Kalonda, A., Mwansa, J., Lukwesa-Musyani, C., Mwaba, J., Mumbula, E.M., et al. (2017) Molecular Characterisation of Methicillin-Resistant Staphylococcus aureus (MRSA) Isolated at a Large Referral Hospital in Zambia. The Pan African Medical Journal, 26, 108.</mixed-citation></ref><ref id="scirp.120529-ref48"><label>48</label><mixed-citation publication-type="other" xlink:type="simple">Chishimba, K., Hang’ombe, B.M., Muzandu, K., Mshana, S.E., Matee, M.I., Nakajima, C., et al. (2016) Detection of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli in Market-Ready Chickens in Zambia. International Journal of Microbiology, 2016, Article ID: 5275724. https://doi.org/10.1155/2016/5275724</mixed-citation></ref><ref id="scirp.120529-ref49"><label>49</label><mixed-citation publication-type="other" xlink:type="simple">Mainda, G., Bessell, P.B., Muma, J.B., McAteer, S.P., Chase-Topping, M.E., Gib-bons, J., et al. (2015) Prevalence and Patterns of Antimicrobial Resistance among Escherichia coli Isolated from Zambian Dairy Cattle across Different Production Systems. Scientific Reports, 5, Article No. 26589. https://doi.org/10.1038/srep12439</mixed-citation></ref><ref id="scirp.120529-ref50"><label>50</label><mixed-citation publication-type="other" xlink:type="simple">Chiyangi, H., Muma, B., Malama, S., Manyahi, J., Abade, A., Kwenda, G., et al. (2017) Identification and Antimicrobial Resistance Patterns of Bacterial Enteropathogens from Children Aged 0 - 59 Months at the University Teaching Hospital, Lusaka, Zambia: A Prospective Cross-Sectional Study. BMC Infectious Diseases, 17, Article No. 117. https://doi.org/10.1186/s12879-017-2232-0</mixed-citation></ref><ref id="scirp.120529-ref51"><label>51</label><mixed-citation publication-type="other" xlink:type="simple">Kalungia, A.C., Burger, J., Godman, B., de Oliveira Costa, J. and Simuwelu, C. (2016) Non-Prescription Sale and Dispensing of Antibiotics in Community Pharmacies in Zambia. Expert Review of Anti-infective Therapy, 14, 1215-1223.  
https://doi.org/10.1080/14787210.2016.1227702</mixed-citation></ref><ref id="scirp.120529-ref52"><label>52</label><mixed-citation publication-type="other" xlink:type="simple">Mudenda, S., Hankombo, M., Saleem, Z., Sadiq, M.J., Banda, M., Munkombwe, D., et al. (2021) Knowledge, Attitude, and Practices of Community Pharmacists on Antibiotic Resistance and Antimicrobial Stewardship in Lusaka, Zambia. Journal of Biomedical Research &amp; Environmental Sciences, 2, 1005-1014.  
https://doi.org/10.37871/jbres1343</mixed-citation></ref><ref id="scirp.120529-ref53"><label>53</label><mixed-citation publication-type="other" xlink:type="simple">Zulu, A., Matafwali, S.K., Banda, M. and Mudenda, S. (2020) Assessment of Knowledge, Attitude and Practices on Antibiotic Resistance among Undergraduate Medical Students in the School of Medicine at the University of Zambia. International Journal of Basic &amp; Clinical Pharmacology, 9, 263-270.  
https://doi.org/10.18203/2319-2003.ijbcp20200174</mixed-citation></ref><ref id="scirp.120529-ref54"><label>54</label><mixed-citation publication-type="other" xlink:type="simple">Raosoft.com (2012) Sample Size Calculator. Raosoft, Inc., Page 1 of 1 Sample Size Calculator. http://www.raosoft.com/samplesize.html</mixed-citation></ref><ref id="scirp.120529-ref55"><label>55</label><mixed-citation publication-type="other" xlink:type="simple">Kalonga, J., Hangoma, J., Banda, M., Munkombwe, D. and Mudenda, S. (2020) Antibiotic Prescribing Patterns in Paediatric Patients at Levy Mwanawasa University Teaching Hospital in Lusaka, Zambia. International Journal of Pharmacy and Pharmacology, 4, 1-9.  
https://1library.net/document/yn44611z-antibiotic-prescribing-patterns-paediatric-patients-mwanawasa-university-teaching.html   
https://doi.org/10.31531/2581-3080.1000138</mixed-citation></ref><ref id="scirp.120529-ref56"><label>56</label><mixed-citation publication-type="other" xlink:type="simple">Republic of Zambia Ministry of Health (2020) Zambia Standard Treatment Guideline 2020. https://www.moh.gov.zm</mixed-citation></ref><ref id="scirp.120529-ref57"><label>57</label><mixed-citation publication-type="other" xlink:type="simple">Kurdi, A., Hasan, A.J., Baker, K.I., Seaton, R.A., Ramzi, Z.S., Sneddon, J., et al. (2021) A Multicentre Point Prevalence Survey of Hospital Antibiotic Prescribing and Quality Indices in the Kurdistan Regional Government of Northern Iraq: The Need for Urgent Action. Expert Review of Anti-infective Therapy, 19, 805-814.  
https://www.tandfonline.com/doi/abs/10.1080/14787210.2021.1834852   
https://doi.org/10.1080/14787210.2021.1834852</mixed-citation></ref><ref id="scirp.120529-ref58"><label>58</label><mixed-citation publication-type="other" xlink:type="simple">Gwebu, P.C., Meyer, J.C., Schellack, N., Matsebula-Myeni, Z.C. and Godman, B. (2022) A Web-Based Point Prevalence Survey of Antimicrobial Use and Quality Indicators at Raleigh Fitkin Memorial Hospital in the Kingdom of Eswatini and the Implications. Hospital Practice, 50, 214-221.  
https://pubmed.ncbi.nlm.nih.gov/35450508/   
https://doi.org/10.1080/21548331.2022.2069247</mixed-citation></ref><ref id="scirp.120529-ref59"><label>59</label><mixed-citation publication-type="other" xlink:type="simple">Kiggundu, R., Wittenauer, R., Waswa, J.P., Nakambale, H.N., Kitutu, F.E., Murungi, M., et al. (2022) Point Prevalence Survey of Antibiotic Use across 13 Hospitals in Uganda. Antibiotics, 11, Article 199. https://pubmed.ncbi.nlm.nih.gov/35203802/   
https://doi.org/10.3390/antibiotics11020199</mixed-citation></ref><ref id="scirp.120529-ref60"><label>60</label><mixed-citation publication-type="other" xlink:type="simple">Tadesse, T.Y., Molla, M., Yimer, Y.S., Tarekegn, B.S. and Kefale, B. (2022) Evaluation of Antibiotic Prescribing Patterns among Inpatients Using World Health Organization Indicators: A Cross-Sectional Study. SAGE Open Medicine, 10.  
https://journals.sagepub.com/doi/full/10.1177/20503121221096608   
https://doi.org/10.1177/20503121221096608</mixed-citation></ref><ref id="scirp.120529-ref61"><label>61</label><mixed-citation publication-type="other" xlink:type="simple">Vaughn, V.M., Hersh, A.L. and Spivak, E.S. (2022) Antibiotic Overuse and Stewardship at Hospital Discharge: The Reducing Overuse of Antibiotics at Discharge Home Framework. Clinical Infectious Diseases, 74, 1696-1702.  
https://academic.oup.com/cid/article/74/9/1696/6374407   
https://doi.org/10.1093/cid/ciab842</mixed-citation></ref><ref id="scirp.120529-ref62"><label>62</label><mixed-citation publication-type="other" xlink:type="simple">Chang, Y., Chusri, S., Sangthong, R., McNeil, E., Hu, J., Du, W., et al. (2018) Clinical Pattern of Antibiotic Overuse and Misuse in Primary Healthcare Hospitals in the Southwest of China. PLOS ONE, 14, e0214779.  
https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0214779   
https://doi.org/10.1371/journal.pone.0214779</mixed-citation></ref><ref id="scirp.120529-ref63"><label>63</label><mixed-citation publication-type="other" xlink:type="simple">Peddireddy, M., Mahin, J., Uppu, A. and Padi, S.S.V. (2021) Hospital Antibiotic Prescribing Pattern in General Surgery Specialty: Analysis Based on the WHO Access, Watch and Reserve (AWaRe) Classification. Journal of Pharmaceutical Research International, 33, 7-19.    
https://doi.org/10.9734/jpri/2021/v33i41B32339</mixed-citation></ref><ref id="scirp.120529-ref64"><label>64</label><mixed-citation publication-type="other" xlink:type="simple">Valia, D., Ingelbeen, B., Kaboré, B., Karama, I., Peeters, M., Lompo, P., et al. (2022) Use of WATCH Antibiotics Prior to Presentation to the Hospital in Rural Burkina Faso. Antimicrobial Resistance &amp; Infection Control, 11, Article No. 59.  
https://doi.org/10.1186/s13756-022-01098-8</mixed-citation></ref><ref id="scirp.120529-ref65"><label>65</label><mixed-citation publication-type="other" xlink:type="simple">Kizito, M., Lalitha, R., Kajumbula, H., Ssenyonga, R., Muyanja, D. and Byakika-Kibwika, P. (2021) Antibiotic Prevalence Study and Factors Influencing Prescription of Who Watch Category Antibiotic Ceftriaxone in a Tertiary Care Private Not for Profit Hospital in Uganda. Antibiotics, 10, Article 1167.  
https://doi.org/10.3390/antibiotics10101167</mixed-citation></ref><ref id="scirp.120529-ref66"><label>66</label><mixed-citation publication-type="other" xlink:type="simple">Seni, J., Mapunjo, S.G., Wittenauer, R., Valimba, R., Stergachis, A., Werth, B.J., et al. (2020) Antimicrobial Use across Six Referral Hospitals in Tanzania: A Point Prevalence Survey. BMJ Open, 10, e042819.  
https://bmjopen.bmj.com/content/10/12/e042819   
https://doi.org/10.1136/bmjopen-2020-042819</mixed-citation></ref><ref id="scirp.120529-ref67"><label>67</label><mixed-citation publication-type="other" xlink:type="simple">Yin, J., Li, H. and Sun, Q. (2021) Analysis of Antibiotic Consumption by AWaRe Classification in Shandong Province, China, 2012-2019: A Panel Data Analysis. Frontiers in Pharmacology, 12, Article ID: 790817.  
https://doi.org/10.3389/fphar.2021.790817</mixed-citation></ref><ref id="scirp.120529-ref68"><label>68</label><mixed-citation publication-type="other" xlink:type="simple">Nguyen, N.V., Do, N.T.T., Nguyen, C.T.K., Tran, T.K., Ho, P.D., Nguyen, H.H., et al. (2020) Community-Level Consumption of Antibiotics According to the AWaRe (Access, Watch, Reserve) Classification in Rural Vietnam. JAC-Antimicrobial Resistance, 2, dlaa048. https://academic.oup.com/jacamr/article/2/3/dlaa048/5905230   
https://doi.org/10.1093/jacamr/dlaa048</mixed-citation></ref><ref id="scirp.120529-ref69"><label>69</label><mixed-citation publication-type="other" xlink:type="simple">Al-Maliky, G.R., Al-Ward, M.M., Taqi, A., Balkhair, A. and Al-Zakwani, I. (2018) Evaluation of Antibiotic Prescribing for Adult Inpatients at Sultan Qaboos University Hospital, Sultanate of Oman. European Journal of Hospital Pharmacy, 25, 195-199. https://ejhp.bmj.com/content/25/4/195   
https://doi.org/10.1136/ejhpharm-2016-001146</mixed-citation></ref><ref id="scirp.120529-ref70"><label>70</label><mixed-citation publication-type="other" xlink:type="simple">Sánchez Choez, X., Armijos Acurio, M.L. and Jimbo Sotomayor, R.E. (2018) Appropriateness and Adequacy of Antibiotic Prescription for Upper Respiratory Tract Infections in Ambulatory Health Care Centers in Ecuador. BMC Pharmacology and Toxicology, 19, Article No. 46.  
https://bmcpharmacoltoxicol.biomedcentral.com/articles/10.1186/s40360-018-0237-y   
https://doi.org/10.1186/s40360-018-0237-y</mixed-citation></ref><ref id="scirp.120529-ref71"><label>71</label><mixed-citation publication-type="other" xlink:type="simple">Wiedenmayer, K., Ombaka, E., Kabudi, B., Canavan, R., Rajkumar, S., Chilunda, F., et al. (2021) Adherence to Standard Treatment Guidelines among Prescribers in Primary Healthcare Facilities in the Dodoma Region of Tanzania. BMC Health Services Research, 21, Article No. 272.  
https://bmchealthservres.biomedcentral.com/articles/10.1186/s12913-021-06257-y   
https://doi.org/10.1186/s12913-021-06257-y</mixed-citation></ref></ref-list></back></article>