Significant morbidity and mortality are associated with antimicrobial resistance.  Monitoring of antimicrobial medication use is therefore essential. The Access, Watch and Reserve (AWaRe) classification of antibiotics developed by the WHO in 2017 supports antimicrobial stewardship efforts and facilitates monitoring of antibiotic use by institutions and nations. The AWaRe tool classifies antibiotics into three groups, Access, Watch and Reserve to emphasize significance of their appropriate use. The aim of this study was to assess antibiotic prescription patterns within the University of Ghana Medical Centre using the WHO AWaRe classification. The data will serve as baseline data that will enable garnering of key conclusions for an antimicrobial stewardship programme.  A point prevalence survey of in-patients was conducted at the University of Ghana Medical Centre on 16^th October, 2021. Medical records of patients on admission were reviewed to identify those on an antibiotic as at 8am on the day of the survey. Data were extracted from the medical records of the patients using the global point prevalence survey tool. Patient data were assessed by organizing antibiotics by the WHO AWaRe classification, and this data was used to analyze other characteristics of antibiotic usage among these patients. Descriptive analysis was carried out to assess frequency and percentage of antibiotics used at the Hospital.  A total of 52 patient records were reviewed, out of which 41 (78.8%) were prescribed at least one antimicrobial medication. Total frequency of antimicrobials prescribed was 74 where 70.3% (52/74) were parenteral antimicrobials, with 29.7% (22/74) being prescriptions for oral antimicrobials. Among this, 81.1% (60/74) of prescriptions had antibiotics classified by the WHO AWaRe criteria with 66.7% (40/60) antibiotic prescriptions in the Watch category and 33.3% (20/60) antibiotic prescriptions in the Access category. Respiratory and urinary tract infections were the most common infections treated (45.9% and 14.9% respectively), and both infections had high proportions of Watch antibiotic use when compared with the AWaRe classification (76.0% and 81.8% respectively). The most frequently utilized antibiotic from the Access category was clindamycin (40%, 8/20), with ceftriaxone (47.5%, 19/40) being the most frequently utilized in the watch category. The majority of antibiotics prescribed were WHO AWaRe classified. Clindamycin and ceftriaxone were the commonly prescribed antibiotics in the Access and Watch categories respectively.  Findings of this survey should serve as an avenue for University of Ghana Medical Centre to invest in efforts to improve antibiotic allocation and monitoring of AWaRe classified antibiotic data through antimicrobial stewardship programmes.

Key Words: Antibiotics, AWaRe, Point Prevalence Survey, Anti-microbial resistance

Antimicrobial resistance (AMR) has become an extremely relevant topic of modern medicine.  Worldwide, an estimated 4.85 million deaths were attributed to AMR in 2019 and 1.27 million of these were solely attributed to bacterial antibiotic resistance (Murray et al, 2022).  Well-known bacterial threats include methicillin-resistant staphylococcus aureus (MRSA), third-generation cephalosporin resistant E.coli, multi-drug resistant (MDR) tuberculosis, carbapenem-resistant klebsiella, and vancomycin-resistant enterococcus (VRE). MRSA alone is thought to be responsible for over 100,000 deaths per year (Hay et al., 2018).  There is significant morbidity associated with AMR as well, such as longer hospital stays, higher medical costs, longer courses of antibiotics and worse surgical outcomes.  However, the true scope of AMR-associated morbidity and mortality has been difficult to fully quantify (Murray et al., 2019; Towe et al., 2021). The methods by which pathogens develop antimicrobial resistance involve innumerable biochemical survival mechanisms, which make combating them difficult.  In the case of bacteria, some of these mechanisms include reduced antibiotic influx or increased antibiotic efflux, antibiotic target modification and antibiotic inactivation (Sulis et al., 2020); this only begins to scratch the surface.  Another key factor allowing for further antibiotic resistance has been antibiotic misuse by medical providers, allowing for selection of bacteria with more robust genotypic compositions (Darby et al. 2023).  While it may be difficult to understand the true impact of AMR, the current state of the emergence of multi-drug resistant organism (MRDO) suggests a dire need for a change in the arbitrary use of antibiotics. Given the latest trajectory, there is suggestion that by 2050, AMR could cause 10 million deaths annually and result in catastrophic economic impacts, forcing up to 24 million people into poverty (WHO, 2019).

Clearly, awareness of the consequences of poor antibiotic stewardship is critical to maintaining antibiotic efficacy and supporting global health, both today and moving forward into the future.  As a measure to help combat the threat of ever-evolving multi-drug resistant organisms, many organizations have begun initiatives aimed at improving responsible antibiotic use by prescribers.  One similar endeavor by the World Health Organization (WHO) was the development of the AWaRe Classification of antibiotics.  Originally released in 2017 with an update in 2021, the AWaRe classification is an invaluable tool to aid in antibiotic stewardship by stratifying antibiotics into three groups: Access, Watch, and Reserve.  Access antibiotics are those that have a wide range of activity against common pathogens and the 25 most common infections but tend to have lower risk of inferring resistance as compared to antibiotics in other groups.  Watch antibiotics have a higher resistance potential as compared to Access, and in general should be used more sparingly when able. Reserve antibiotics are those that should be accessible, but only used in necessary or reserved scenarios.  An additional category exists titled Not Recommended, mainly for antibiotic combinations whose use is not evidence based (WHO, 2021).

The primary goal of the AWaRe classification is to facilitate the monitoring of antibiotic use by institutions and nations.  In addition to this framework, the WHO 13th General Programme of Work 2019-2023 created a specific goal for the end of 2023 titled: Access >60%, which aims to increase the proportion of Access antibiotics utilized to over 60% globally. According to WHO, there are currently 65 countries tracking AWaRE adherence data. Notably, only 29 of these 65 countries (44.6%) have reached the 2023 goal of 60% or higher Access group usage (WHO, n.d; Adoptaware, n.d).  Ghana does not routinely track AWaRe adherence data, making it difficult to assess antibiotic stewardship. At the University of Ghana Medical Centre (UGMC), this is relevant because unavailability of such information makes it difficult to determine where necessary resources should be appropriated, such as requesting for more culture and sensitivity testing for clients. Understanding and applying classifications such as AWaRe, while being mindful of antibiotic selection is an excellent opportunity to improve patient outcomes which is ethically relevant for the prevention of future AMR. The primary aim of the study was to assess antibiotic prescription patterns within the University of Ghana Medical Centre. This will be a baseline data that enables us to garner key conclusions for antibiotic stewardship programmes in Ghana.

Study design

To obtain the necessary data surrounding antibiotic utilization at UGMC, the institution’s Antimicrobial Stewardship Committee performed a point prevalence survey of in-patients at the UGMC on 16^th October, 2021. The Global Point Prevalence Survey Method was used for data collection which covered in-patients on surgical, medical, obstetrics & gynaecology, emergency, pediatric and neonatal wards.

Study data collection

The Global Point Prevalence Survey tool was used to collect data on antibiotics use in the hospital. For each in-patient, demographic information was collected and patients’ medical records for the period of their admission was reviewed by trained data collectors to identify those on an antibiotic as at 8am on the day of the survey. 

Data Analysis

The patient data was rigorously assessed by categorizing antibiotics according to AWaRe classification and used to evaluate various characteristics of antibiotic usage among the patients.

We investigated the correlation with ward, subspecialty and type of infection.  The analysis also covered the number of antibiotics used per patient and, particularly, the number of AWaRe-classified antibiotics per patient. Data analyses were conducted using Microsoft Excel 2010.

Ethical Approval and Considerations

The data for the study was obtained as part of the routine ward rounds conducted by the Antimicrobial Stewardship Committee at the UGMC. All participants were informed and consented to the review of their medical records. The dataset became part of the records of the Antimicrobial Stewardship Committee at the UGMC, as such its use for the study received a waiver from the University of Ghana Medical Centre Institutional Review Board (UGMC-IRB).

There was a total of 52 patients on all the wards that were surveyed out of which 41 (78.8%) were on at least one antibiotic.  Among these 41 patients on antibiotics, 34 adult patients and 7 paediatric patients; there were 18 male patients, and 22 female patients. (ref table 1).

 

Table 1: Demographic characteristics of patient on Antibiotics

Variables	N (%)	variables	N (%)
In-patients		Ward type
Patients on antibiotics	41(78.9%)	Adult medical ward	25(60.9%)
Patients not on antibiotics	11(21.1%)	Adult surgical ward	9(21.9%)
Sex of patient		Paediatric medical ward	3(7.3%)
Male	18(43.9%)	Newborn medical ward	2(4.9%)
Female	22(53.7%)	NICU	2(4.9%)
unidentified	1(2.4%)	Subspecialty
		internal medicine (subspecialties)	17(41.5%)
Patient type		surgical patients	9(21.9%)
Adult patient	34(82.9%)	paediatric patients	7(17.1%)
Pediatric patient	7(17.1%)	Emergency medicine	6(14.6%)
		obstetrics and gynaecology	2(4.9%)

*NICU – Neonatal Intensive Care Unit

 

 

Use of WHO AWaRe Classification in the facility

With regards to antibiotic use, total frequency of antimicrobials prescribed was 74 where 70.3% (52/74) were parenteral, with 29.7% (22/74) being oral. Among these, 81.1% (60/74) of prescriptions had antibiotics classified by the WHO AWaRe criteria.

Most notably, there was a skew toward the use of Watch antibiotics, with 40 out of the 60 prescriptions with WHO AWaRe classified antibiotics being within this subgroup.  Conversely, there were 20 prescriptions with Access antibiotics and 0 Reserve antibiotics used. 

The patients within our study population received a mean of 1.46 AWaRe-classified antibiotics, and a mean of 1.80 for all prescribed antibiotics (AWaRe classified and those not classified). The most common antibiotic used was ceftriaxone, with 19 uses and belonging to the Watch subgroup.  Other commonly used antibiotics included clindamycin in the Access subgroup (with 8 uses); meropenem in the Watch subgroup (with 5 uses); and cefuroxime in the Watch subgroup (with 4 uses). 

The percentage of Watch antibiotics as a proportion of all antimicrobials used in this population was 54.1%, increasing to  66.6% when calculated as a proportion of all AWaRe-classified antibiotics used.  Thus, percentage of Access antibiotics as a proportion of all antimicrobials used in this population was 27.0% and 33.3% when calculated as a proportion of all AWaRe-classified antibiotics used (ref table 2). 

 

Table 2: Use of WHO AWaRe classified Antibiotics at UGMC

Total antimicrobials Used 74(100%)
Variables	N (%)	Variables	N (%)
Route of administration		AWaRE classification by Neonatal medical ward
Parenteral	52 (70.3%)	Watch	2 (50%)
Oral	22 (29.7)	Access	2 (50%)
AWaRE classification		AWaRE classification by NICU
Watch	40 (66.7%)	Watch	1 (25%)
Access	20 (33.3)	Access	3 (75%)
Reserve	0
AWaRE classification by ward		AWaRE classification by internal medicine
Adult Medical Ward	33 (55%)	Watch	17 (70.8%)
Adult Surgical Ward	14 (23.3%)	Access	7 (29.2%)
Pediatric Medical Ward	5 (8.3%)	AWaRE classification by Surgery
Neonatal Medical Ward	4 (6.7%)	Watch	8 (57.1%)
Neonatal Intensive Care Unit	4 (6.7%)	Access	6 (42.9%)
AWaRE classification by Specialty		AWaRE classification by Emergency medicine
Internal Medicine (Cardiology + General):	24 (40%)	Watch	7 (100%)
Surgery	14(23.3%)	Access	0
Emergency Medicine	7 (11.7)	AWaRE classification by paediatrics /Neonatal /NICU
Pediatrics/Neonatal/NICU	13(21.7%)	Watch	7 (53.8%)
OBGYN	2 (3.3%)	Access	6 (46.2%)
AWaRE classification by Activity		AWaRE classification by OBGYN
Medical	40 (66.7%)	Watch	1 (50%)
Surgical	16 (26.7%)	Access	1 (50%)
Intensive care	4 (6.7%)
AWaRE classification by AMW		AWaRE classification by medical activity
Watch	25 (75.8%)	Watch	30 (75%)
Access	8 (24.2%)	Access	10 (25%)
AWaRE classification by ASW		AWaRE classification by surgical activity
Watch	8 (57.1%)	Watch	9 (56.2%)
Access	6 (42.9%)	Access	7 (43.8%)
AWaRE classification by PMW		AWaRE classification by intensive care activity
Watch	4 (50%)	Watch	1(25%)
Access	4 (50%)	Access	3(75%)
*OBGYN – Obstetrics and gynaecology, AMW – Adult Medical Ward, ASW – Adult Surgical Ward, PMW – Pediatric Medical Ward, NICU – Neonatal intensive care unit, Neonatal Medical Ward

 

When analyzing AWaRe antibiotic usage relative to ward and subspecialty, medical wards tended to use more Watch antibiotics rather than surgical wards.  For example, within the AMW, 75.8% of antibiotics used were among the Watch subgroup.  Meanwhile, on the ASW, 57.1% of antibiotics used were among the Watch group.  Other less-represented wards revealed the following:  PMW with 80%, NMW with 50%, and NICU with 25% of Watch antibiotics among all these subgroups.  This was reflected similarly among subspecialties, where 70.8% of the antibiotics used were among the Watch subgroup.  Surgical specialties used 57% Watch antibiotics, emergency medicine used 100% Watch antibiotics, Paediatrics used 53% Watch antibiotics and, lastly, Obstetrics and Gynaecology used 50% Watch Antibiotics.

Type of infection and AWaRe-classified antibiotic used for treatment.

Based on type of infection, respiratory and urinary infections were the most common infections treated (45.9% and 14.9% respectively) and within this, both had high proportions of Watch antibiotic use when treated with AWaRe-classified antibiotics (76.0% and 81.8% respectively).  (ref table 3).

 

Table 3: Type of infection and AWaRe-classified antibiotic used for treatment

Variables	N (%)	Variables	N (%)
AWaRE classification by site infection		AWaRE classification by Gastrointestinal
Respiratory	25 (41.7%)	Watch	3 (42.8%)
Urinary tract infection	11 (18.3%)	Access	4 (57.1%)
No determined site (NDS)	5 (8.3%)	AWaRE classification by Neonatal
Gastrointestinal	7 (11.7%)	Watch	1 (25%)
Neonatal	4 (6.7%)	Access	3 (75%)
Genitourinary Obstetric	3 (5.0%)	AWaRE classification by Genitourinary Obstetric
Skin, Soft Tissue, Bone and Joint	3 (5.0%)	Watch	2 (66.7)
Cardiovascular (CVS)	2 (3.3%)	Access	1 (33.3)
AWaRE classification by Respiratory infection		AWaRE classification by SSTBJ
Watch	19 (76%)	Watch	1 (33.3)
Access	6 (24)	Access	2 (66.7)
AWaRE classification by UTI		AWaRE classification by cardiovascular
Watch	9 (81.8%)	Watch	1 (50%)
Access	2 (18.2%)	Access	1 (50%)
AWaRE classification by NDS
Watch	4 (80%)
Access	1 (20%)
*SSTBJ - Skin, Soft Tissue, Bone and Joint, UTI - Urinary tract infection,  NDS - No determined site

 

 Antibiotics and AWaRe Classification

Based on type of antibiotics, clindamycin and ceftriaxone were the most commonly utilized antibiotics under the Access and Watch categories respectively. Clindamycin under the Access category formed 40% of all Access antibiotics utilized and Ceftriaxone formed 47.5% of all Watch antibiotics (ref. table 4).

 

Table 4: WHO AWaRe Classification of antibiotics

Name of Antibiotics	Access	Watch
	N (%)	N (%)
Amoxicillin and enzyme inhibitor	3(15%)
Ampicillin	2(10%)
Azithromycin		3(7.5%)
Benzylpenicillin	1(5%)
Cefotaxime		1(2.5%)
Ceftazidime		1(2.5%)
Ceftriaxone		19(47.5%)
Cefuroxime		4(10%)
Ciprofloxacin		1(2.5%0
Clindamycin	8(40%)
Cloxacillin	1(5%)
Gentamicin	2(10%)
Levofloxacin		3(7.5%)
Meropenem		5(12.5%)
Metronidazole	1(5%)
Nitrofurantoin	1(5%)
Rifampicin		3(7.5%)
Sulfamethoxazole and trimethoprim	1(5%)

The results of the study reveal key areas for intervention regarding UGMC’s antimicrobial stewardship.  The most striking and obvious finding is the proportion of antibiotics utilized from the Watch group.  As previously stated, the WHO General Programme 2019-2023 defined a clear aim to improve the use of lower-risk antibiotics. The aim of the Programme is to have 60% of all antibiotics utilized to belong to the Access group.  However, the point prevalence survey conducted indicates only 33.3% of Access antibiotic use, with 66.6% belonging to the Watch group instead.  A similar study found the Watch group accounted for the majority (53.6%), followed by the Access (36.4%) antibiotic group (Islam et al., 2022). Fortunately, there was no evidence of Reserve subgroup usage in our data pool, suggesting that there are minimal instances of these riskier antibiotics being given. The evidence available from the pharmacy indicates that this class of antibiotics was not available in stock at the time of the study. Again, antibiotics in the Reserve class are expensive and most patients are unable to afford them. Therefore, prescribers knowing this will mostly not prescribe Reserve antibiotics. However, there is clearly a large room for improvement in the prescription of low-risk antibiotics.  Further, we provide insight into areas where this potential is most pronounced, such as on medical wards, within medical subspecialties, and for certain infectious sites.

Patients within the Adult Medical Ward were the most represented within our study, but also had the most pronounced disparity in low-risk antibiotic use with 75.8% Watch antibiotics as discussed previously.  Other groups tended to use more Access antibiotics, however some of these data may be limited by sample size.  Similarly, Internal medicine subspecialties were found to utilize Watch antibiotics to treat 70.8% of the infections where they used AWaRe-classified antibiotics.  An additional group of concern were patients who were put on emergency medicine, with 100% of their antibiotics being Watch-classified.  Possible reasons for this discrepancy between other wards and subspecialties are the types of infections that are being treated and the acuity of patients with infections that these doctors treat.  A patient whose primary reason for hospitalization is infection may be more likely to have severe infection or resistant infection. It's important to consider the challenges faced in the emergency department, where patients often arrive with undifferentiated symptoms, requiring broad-spectrum antibiotic coverage. However, the ability to narrow down antibiotic choices based on culture data throughout the hospital stay is crucial in combating antimicrobial resistance. Without access to such data, doctors may face challenges in appropriately tailoring antibiotic treatment, which can contribute to worsening antimicrobial resistance patterns

There is a need to consider the types of infections being treated with AWaRe antibiotics. Respiratory and urinary tract infections (UTIs) are commonly treated with "Watch"-classified antibiotics, with 76.0% of respiratory infections and 81.8% of UTIs being treated with these antibiotics. This is partly due to guidelines often recommending ceftriaxone as a first-line therapy for in-hospital community-acquired pneumonia and UTI treatment, and ceftriaxone has been classified as a "Watch" antibiotic according to AWaRe classification.

(Metlay et al., 2019; Gupta et al., 2011).  Indeed, this is consistent with our study population which saw ceftriaxone as the most prevalent antibiotic choice.  No determined site (NDS) also yielded a high proportion of Watch antibiotic usage, which may be expected due to the generally broad nature of antibiotic therapy in the setting of an infection with an unidentified source.  Other infectious sources yielded lower Watch utilization, such as gastrointestinal sources of infection (42.9% Watch use), neonatal infections (25% Watch use), obstetrics-associated genitourinary infections (66.7% Watch use), skin, soft-tissue, bone and joint infection (33.3% Watch use), and cardiovascular infections (50% Watch use).  However, it is difficult to ascertain the reasoning behind all of these antibiotic choices without specific clinical context.

In interpreting the study results, these limitations need to be considered. The study is a cross-sectional point prevalence survey among 52 patients that were on admission at the hospital on a particular day within a specific time. This may not be a true representation of antibiotic prescription trends in the hospital. Secondly, at the time of the data collection, pneumonia was at its peak in Ghana. As such, this could be an influencing factor on the high prevalence of infections, frequent prescription and use of antibiotics. Lastly, the hospital was new and was in the process of building its operational systems. For instance, the hospital had no antibiotic prescription guidelines. Hence prescribers followed guidelines that they were familiar with. Again, the hospital microbiology laboratory was not in operation at the time of data collection. Microbiology tests were outsourced which caused a lot of delays and less reliance on test results during the treatment and prescription of antibiotics for infections.

The majority of antibiotics prescribed were WHO AWaRe-classified. However, inadequate specific culture and microbial susceptibility tests, as is the general practice in-country, makes it difficult to ascertain if the chosen antibiotics were required for the specific pathogens. This, in turn, makes the prescriber unable to safely de-escalate to an antibiotic with less antimicrobial resistance potential.  Findings of this study should serve as an avenue for University of Ghana Medical Centre and other similar facilities to invest in efforts to improve antibiotic allocation and monitoring of AWaRe classified antibiotic data through antimicrobial stewardship programme.  By doing so, the hope is to spark new efforts to contain antimicrobial resistance and improve the outcomes of patients now, but also improve future potential.

Conflict of Interest

The authors have no conflict of interest.

Funding

No funding was provided for this study.

Data Availability Statement

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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