A Situation Analysis of the Capacity of Laboratories in Zambia to Conduct Surveillance of Antimicrobial Resistance: Strengths, Weaknesses, Opportunities, and Challenges

1. Introduction

Antimicrobial resistance (AMR) occurs when bacteria, viruses, fungi, and parasites do not respond to antimicrobial drugs in animals or humans, thereby allowing the organism to survive in the host despite exposure to sufficient doses [1,2,3]. Antimicrobial resistance (AMR) has been spreading extensively worldwide and remains a serious threat to public health globally [4,5]. The effects of AMR cut across health, environmental and economic paradigms, making its impact more pronounced [6,7,8]. This phenomenon has been worsened by a lack of surveillance and diagnostic systems, especially in low-income settings, where large quantities of antimicrobial agents are used [9,10,11]. With the problem expected to escalate, it is estimated that there will be 10 million deaths per year globally due to AMR [1,12].

The deficiency in laboratory capacity and systems to conduct AMR surveillance has been linked to many factors, including lack of funding, inadequate training of healthcare personnel, lack of training in antimicrobial stewardship (AMS), shortages of laboratory consumables, and a lack of necessary laboratory equipment [13]. Consequently, some laboratories in low-resource settings face challenges regarding infrastructure, technical issues, and behavioural change in implementing clinical bacteriology testing [14]. Additionally, evidence has shown that the role of laboratories in the surveillance of AMR is affected by the absence of antibiograms, a lack of quality management systems, a lack of proficiency testing, lack of guidelines and standard operating procedures (SOPs), among other challenges [6,14,15,16,17]. A study that was done at a teaching hospital in Ghana highlighted the importance of cumulative antibiograms in AMS programmes after its communication to clinicians and subsequent monitoring influenced prescribing indicators [18].

Strengthening laboratory surveillance of AMR is essential to address escalating drug-resistant infections [19,20,21]. Studies have shown an improvement in AMR surveillance after improving the capacity of laboratory testing [6,10,22]. Additionally, laboratory findings help clinicians to make decisions regarding the treatment of particular infections [13,23,24]. This promotes the principles of diagnostic stewardship through which laboratories contribute to the appropriate diagnosis and treatment of infections [25,26,27,28]. Hence, through diagnostic stewardship, antimicrobials are prescribed based on the right test, to the right patient, which prompts the right action, leading to efficient use of resources, improved use of antimicrobials, and a reduction in AMR [25,26,29]. However, there are some concerns about clinicians underutilizing clinical microbiology laboratory data when making clinical decisions [30]. Substantial investment has to be made to improve laboratory capacity to conduct AMR surveillance, especially in low-income and middle-income countries (LMICs), which have the highest burden of diseases [31,32].

Addressing AMR requires systematic instigation and implementation of AMS programs in healthcare facilities [33,34,35]. Through AMS programs, laboratory staff can be educated and trained in good laboratory practices that aim to promote the generation of high-quality and reliable test data, reduction in antimicrobial use, and reduction in AMR [18,36,37,38]. AMS programs can facilitate education and capacity building among laboratory scientists, leading to enhanced antimicrobial susceptibility testing (AST), enhanced culture and susceptibility reports, accurate rapid diagnostic testing, and improved alert and surveillance systems [39]. Furthermore, collaborations that foster action-oriented and multidisciplinary facility AMS programs can lead to the successful implementation of AMS activities [40,41]. Notably, AMS interventions lead to improved prescribing practices of antimicrobials and lead to improved patient outcomes [42,43,44,45,46].

Zambia is a country in the sub-Saharan African (SSA) region with a reportedly high burden of infectious diseases [47,48,49]. Consequently, the presence of drug-resistant pathogens in healthcare facilities has been reported in several studies [50,51,52,53,54,55,56,57,58]. The Antimicrobial Resistance Coordinating Committee (AMRCC) hosted at the Zambia National Public Health Institute (ZNPHI) has been promoting the establishment and strengthening of AMR surveillance across the country [59,60]. The ZNPHI has supported One Health AMR surveillance through the 2019 Zambia Integrated Surveillance Framework for Antimicrobial Resistance [59]. However, there is a paucity of information on the capacities of laboratories to conduct AMR surveillance in Zambia. Therefore, this study assessed the capacity to conduct bacteriology, AMR testing and surveillance in seven faith-based hospitals in the Zambia to contribute to available data on the subject. It was envisaged that the findings of this assessment would be used to strengthen AMR surveillance in faith-based hospital-affiliated laboratories in Zambia.

2. Results

This study enrolled seven faith-based hospitals in five provinces of Zambia. All the seven hospitals surveyed had physical laboratory infrastructure. However, they all scored below 50% regarding their ability to conduct basic medical bacteriology and capacity to test for AMR, indicating low capacity to conduct AMR surveillance (Figure 1). The overall score was 39%.

This study found that an average score of 41% was obtained for all the assessed indicators thereby demonstrating the low capacity of hospitals to conduct medical bacteriology and AMR testing (Figure 2). The hospitals scored low (0-48%) in 10 indicators while moderate (51-74%) in four indicators (Figure 2). Low scores (0-48%) were recorded by the assessed laboratories in 10 indicators while moderate scores (51-74%) in four indicators were recorded (Figure 2). The highest average score was 74% on data management with only St. Francis Mission Hospital (SFMH), (Macha Mission Hospital (MaMH), and Chikankata Mission Hospital (CMH) having performed well. All the surveyed hospitals scored 0% in quality control of ASTs (Figure 2). Only CMH performed well regarding the safety audit. Finally, only MMH had full capacity to run LIS and to conduct identification quality control (Figure 2). Individual facility scores are also shown in the Supplementary Material (S1).

3. Discussion

This study was a situation analysis involving a baseline assessment of the capacity of laboratories to conduct medical bacteriology, AMR testing and surveillance in faith-based hospitals in Zambia. We found that all seven faith-based hospitals exhibited limited capacity to conduct AMR surveillance, with an overall score of 39%. Additionally, an average score of 41% was recorded based on the indicators that were assessed. Despite having physical laboratory infrastructure across all seven hospitals, only three had good capacity to perform data management, only one hospital had a well-functioning LIS, and only one hospital met the safety standards required of a microbiology laboratory. Therefore, our findings demonstrated a strong need to strengthen the capacity of laboratories to perform bacteriology, AMR testing and surveillance.

Our study found a low capacity of faith-based hospital-affiliated laboratories to conduct medical bacteriology, AMR testing, and implementation of laboratory-based AMR surveillance in Zambia. Our findings are evidenced by the low overall score regarding the indicators used in assessing the capacity of laboratories to test for AMR and perform all bacteriological processes. These findings align with those reported in other studies [6,61,62]. A recent study conducted in Zambia in secondary and tertiary hospitals found an overall capacity of 52%, with the highest-scoring hospital having scored 63% and the lowest having scored 38% [63]. Another study in Burkina Faso found that an overall capacity to conduct AMR surveillance was 40% across 18 laboratories, with the highest laboratory scoring 58% and the lowest 26%, indicating a low capacity to conduct QMS and AMR surveillance [64]. The low capacity of laboratories to conduct bacteriological tests and AMR testing affects the surveillance of AMR. This problem affects many African countries [65]. In Africa, the lack of capacity of laboratories to conduct most microbiology tests affects the validity, usefulness, and trustworthiness of data generated from the surveillance systems [66].

The present study found that none of the surveyed laboratories had full capacity to test for AMR due to challenges including sub-optimum laboratory conditions, equipment unavailability, lack calibration and maintenance, inconsistent or lack of temperature monitoring, lack of an autoclave and inconsistent or absent inventory management. Our findings resonate with another study conducted in Ethiopia where, despite the availability of laboratories, there was a lack of basic equipment and consumables to conduct AMR testing [6]. Another study in Kenya reported similar findings where nearly one-third of the healthcare facilities examined did not offer bacterial culture testing, and only a meagre 16.9% conducted AST [61]. This was due to poor access to LIS, low participation in external quality assessment programs for cultures, severe infrastructural gaps and lack of equipment [61]. In Rwanda, critical gaps in equipment and supplies were found in district hospitals, similar to those found in our study [67]. Our findings and those reported in other African countries conform with earlier findings that there is a lack of proper reliable, cost-effective and easy-to-use AMR diagnostic tools, particularly in routine diagnostic laboratories [65,68]. Additionally, there are few reports of major testing gaps for AMR in other regions with currently available data comprehensively describing AMR trends [69]. These differences could be attributed to differences in the setup and development of healthcare systems, particularly those in the African region severely impacted by financial constraints and infrastructural challenges.

Our study revealed that only Mwandi Mission Hospital had full LIS capacity to run electronic data management systems. The rest of the surveyed hospitals could not run LIS, demonstrating a critical disadvantage in the processing and storage of information. Our findings corroborate those reported in Kenya, where most laboratories scored low on the LIS component of the indicators [61]. Evidence has shown that LIS is generally poor in most LMICs, affecting AMR surveillance [32]. Studies have reported that laboratories need to develop and implement their LIS to reduce identification errors, improve data security and protection, and promote the efficiency reported of results [70,71,72].

The current study found that only three hospitals, including Chikankata, St. Francis, and Macha Mission Hospitals had good data management capacity and scored well in patient and specimen identification, specimen requisition forms, order entry, culture observations, AST data reporting, data backup and security, and AMR data sharing. Hence, most hospitals in this study could not perform good data management. These findings were also echoed in a study in Ethiopia, where data capture and transmission challenges were cited as common problems in implementing AMR surveillance work [73]. Additionally, a comprehensive review underscored the necessity for prompt intervention to address the issues related to data infrastructure and financial stability [74]. This is crucial to maintain the effectiveness and sustainability of surveillance initiatives. Moreover, it has been established that data systems for AMR surveillance are essential for fostering unified public health measures and guaranteeing the distribution of sufficient feedback [74]. Our findings agree with a previous study done in Nepal, where data generated from facilities was inconsistent, incomplete and delayed, thereby causing challenges in data transmitted to the national level for action [22]. In contrast, a study in Ethiopia described effective data management after deliberate efforts to establish a surveillance system [75]. These differences could be due to an absence of systems for capturing AMR data.

Our study found that all the surveyed hospitals could not perform quality assurance, including the basics of the quality management system (QMS), staff competency assessments, troubleshooting mechanisms and external QA. Implementation of QMS dictates that health facilities align themselves to national and international requirements of quality assurance which eventually enables a culture of quality in all sectors of healthcare [17]. A study among 18 laboratories in Burkina Faso also reported a low performance of laboratories to conduct QMS and external QA [64]. Not surprisingly, our study found that all the surveyed hospitals could not perform media QC, identification QC, and AST QC. Similarly, a study in Togo had findings in which the AST QC was very low [76]. In contrast to our findings, a study conducted in Burkina Faso found that most (76.5%) facilities had a good capacity to conduct AST QC [64]. In keeping with the findings from the Burkina Faso study [64], a study conducted in Kenya reported good performances (≥80%) in QA and a score of 81.1% in AST QC was reported [61]. Intriguingly, evidence has shown that the implementation of QMS in laboratories enhances patient safety [77].

All the surveyed hospitals in the current study did not have the full capacity to implement bacteriological identification methods. The methods used were not supported by SOPs, protocols and flow charts. These findings are worrying because the lack of proper identification of microorganisms affects the management, treatment and control of infections [78]. The lack of SOPs, protocols, and flow charts has also been reported in other countries, especially in low-resource settings [14,16,17]. The implementation of clinical bacteriology improves patient management, provides valuable surveillance for local antibiotic treatment guidelines and supports the containment of AMR as well as the prevention and control of hospital-acquired infections [14]. Additionally, SOPs provide instructions on how to isolate and identify pathogens, assign bacteria to a specific group, interpretation of results, and recommend panels of antibiotics for AST for a particular pathogen [16,79]. Hence, gaps in basic identification methods and a lack of SOPs negatively affect the process of bacteriology. There is an urgent need to strengthen laboratory detection of pathogens through the strengthening of laboratory capacity to conduct bacteriology [78]. Therefore, the need for SOPs in bacteriological processes must be emphasized in maintaining the accuracy, consistency, and quality of data [79].

Our study revealed that none of the seven hospitals had the full capacity to perform maintenance of discs and strips, inoculum preparation, incubation, reading and interpreting results and breakpoints standards. Hence, this deficiency highlights the potential problems associated with adhering to the established guidelines provided by the Clinical and Laboratory Standards Institute (CLSI) and/or the European Committee on Antimicrobial Susceptibility Testing (EUCAST) breakpoints and AST expert rules for the priority pathogens. These challenges are mostly seen in LMIC where securing the supply chain and investing in adapted equipment, diagnostics, and reagents adapted to the environmental, logistic, and financial challenges is difficult to sustain [80]. In addition, none of the seven hospitals in the present study had the full capacity to perform specimen collection, transport, management, and processing of blood, urine, and stool cultures. Many studies have documented challenges in conducting routine bacteriological diagnostics and subsequent AST, mainly in low- and middle-income countries [13,69,73,75,81].

Our study found that only Chikankata Mission Hospital had a good capacity for the safety requirements of a microbiology laboratory that must be involved in AMR testing and surveillance. Zimba Mission Hospital was at borderline (79%) to attain good capacity regarding safety audits in the microbiology laboratory. Poor safety standards in laboratories have the potential to put laboratory workers at increased risk of contracting laboratory-acquired infections [82]. The challenges in biosafety and biosecurity have been documented in other countries, outlining the lack of safety assurance leading to unsafe handling of infectious materials in the laboratory [83,84]. Ultimately, this affected the implementation of AMR programs in health facilities and laboratories [85,86]. Our findings and those reported in other studies indicate the need to conduct frequent assessments and monitoring of biosafety and biosecurity in laboratories [87]. Hence, there is a critical need to strengthen biorisk management in laboratories to reduce and tackle infections [82,88].

We found that none of the seven assessed laboratories had an antibiogram. The absence of antibiograms creates a huge gap in promoting targeted antimicrobial treatment. Due to the absence of antibiograms in health institutions, it is not feasible to evaluate the extent of pathogen resistance to antimicrobials. Notably, the use of antibiograms enhances the rational use of antimicrobials and promotes AMS [18,89]. Additionally, antibiograms are used to detect and monitor current patterns in AMR [90]. Consequently, the lack of antibiograms in clinical laboratories can have substantial implications for patient treatment and public health. The significance of antibiograms in the presence of significant AMR in Gram-negative bacteria was underscored, focusing on their role in directing antibiotic treatment and managing multi-drug resistant organisms [91]. Notably, antibiograms are essential in enhancing AMS, infection control, and rational antimicrobial therapy [18,92]. A study in Ghana highlighted the importance of antibiograms’ ability to support empirical clinical decision-making and enhance infection prevention highlighting their value in laboratories [93].

The gaps identified in our study demonstrate the need to develop strategies that should be used to improve the surveillance of AMR in Zambia. In addition, none of the surveyed hospitals had an AMS committee to champion heightened AMR surveillance. Therefore, we believe setting up AMS teams is critical to improving the surveillance of AMR, similar to earlier publications [20,94,95,96,97,98,99,100]. Additionally, AMS and surveillance programs can help in capacity building and mentorship of laboratory personnel regarding microbiology and AMR surveillance [39]. Strengthening laboratory capacity to monitor and conduct AMR surveillance potentially reduces the development and spread of AMR [101,102,103].

We are aware that our study had limitations. First, this was a cross-sectional study relying on self-reporting by respondents and is prone to recall biases. Second, this study was conducted in faith-based hospitals. Hence, generalisation of the findings must be made with caution as the findings may not reflect what is obtained in public and private hospitals. Consequently, the study findings may not represent all the faith-based hospitals in Zambia as the study was done in five out of ten provinces in Zambia. However, our findings are vital and can be used to identify opportunities and gaps that can be leveraged on to strengthen AMR surveillance in faith-based hospitals in Zambia. Additionally, as a starting point to strengthen AMR testing and surveillance in the surveyed hospitals, the presence of a physical laboratory infrastructure in all seven hospitals is very cardinal.

4. Materials and Methods

4.1. Study Design, Period, and Setting

We conducted a cross-sectional exploratory study in seven faith-based hospitals in Zambia from February 2024 to April 2024. The hospitals are located in five different provinces as follows: Chikankata Mission Hospital (CMH) in the Chikankata District, Macha Mission Hospital (MaMH) in the Choma District, Zimba Mission Hospital (ZMH) in the Zimba District of the Southern Province; Mwandi Mission Hospital (MMH) in Mwandi District of the Western Province; St. Francis Mission Hospital (SFMH) in Katete District of the Eastern Province; St. Dominic’s Mission Hospital (SDMH) in Ndola District of the Copperbelt Province; and Mukinge Mission Hospital (MuMH) in Kasempa District of the Northwestern Province. These faith-based hospitals were chosen because they provide medical and surgical services to many Zambian people, largely in remote places (Figure 3). Additionally, the sites were chosen because they are under the ambit of the Churches Health Association of Zambia (CHAZ), which will strengthen the microbiology activities of these hospitals to help scale up their capacity to conduct bacteriology, AMR testing and surveillance. In our study, a faith-based hospital was defined as a hospital that is supported by or affiliated with a Christian religious group such as Catholics, Anglicans, Presbyterians, and Protestants.

4.2. Sample Size and Sampling Technique

We selected seven faith-based hospitals using the purposive sampling method to conduct a baseline assessment study on the capacity of laboratories to conduct basic medical bacteriology, AMR testing and surveillance. Purposive sampling has been used in studies similar to the current study because it helps collect comprehensive, specific information based on the study objectives [62,104]. We purposefully selected four key informants working in the microbiology section of the laboratory in the surveyed hospitals. This gave us a total of 28 key informants across the seven hospitals. The key informants included the laboratory manager, the quality control officer, and bench personnel.

4.3. Data Collection

Data were collected using a Microsoft Excel sheet version of the self-scoring Laboratory Assessment of Antibiotic Resistance Testing Capacity (LAARC) questionnaire [105]. The tool is validated and recommended by the Centers for Disease Control and Prevention (CDC) to be used for evaluating laboratories proficient in conducting bacteriologic techniques and other related quality processes that require accurate and reliable AMR detection and reporting [105]. The LAARC questionnaire has 15 modules, each containing 3 to 10 indicators. Additionally, each indicator contains closed-ended questions to which laboratory personnel respond [105].

The 15 modules include Module 0, called General (laboratory demographics, test menu and workload, ST/AMR workload and methods, laboratory staff education and training, QMS mentoring programs, and accreditation and certification); Module 1: Facility (laboratory facility, general equipment availability, media preparation equipment availability, equipment calibration records, thermometers, temperature and atmosphere monitoring, autoclave management, instrument availability and maintenance, and inventory and stock outs); Module 2: Laboratory Information System (LIS) (demographic data fields, specimen data fields, culture observation data fields, AST data fields, reports and data transfer capabilities, and interface connectivity); Module 3: Data Management (patient and specimen identification, specimen requisition form, order entry, culture observations, AST results reporting, data backup and security, and AMR data sharing); Module 4: Quality Assurance (QA) (quality structure/basics, laboratory staff education/training/competency, troubleshooting, problem solving, and route cause analyses, and external quality assessment (EQA); Module 5: Media Quality Control (QC Media) (media preparation SOPs, general media preparation, distilled/deionized water preparation, routine media QC, Mueller Hinton media preparation and QC, and blood culture bottles preparation and QC); Module 6: Identification QC (QC ID) (gram stain QC and reagent labeling and storage, QC of individual biochemical methods, QC of enteric serology, QC of commercial ID kids and automated ID systems); Module 7: Antimicrobial Sensitivity Testing QC (QC AST) (routine AST references strains, special AST reference strains, QC of disc diffusion methods, QC of gradient strip AST methods, and QC of automated AST systems); Module 8: Specimen (specimen management, specimen rejection, blood specimen collection and transportation, urine collection specimen and transportation, and stool specimen collection and transportation); Module 9: Processing (blood culture processing, manual blood culture systems, urine culture, stool cultures for Salmonella and Shigella); Module 10: Identification methods and Standard Operating Procedures; Module 11: Basic AST (antibiotic disc and gradient strips maintenance, inoculum preparation, inoculum/incubation, reading AST results, interpreting AST results, and breakpoints standards; Module 12: AST expert rules (expert rules for Salmonella, gram negatives and beta-lactams breakpoints, phenotypic ESBL testing, phenotypic carbapenamase testing, colistin testing, expert rules for Staphylococcus aureus, general considerations and expert rules for Streptococcus pneumoniae, inducible clindamycin resistance testing, and expert rules for cerebrospinal fluid); Module 13: AST policy (AST panels, cumulative antibiograms, and AST policy); and Module 14: Safety (biosafety equipment, personal protective equipment, biosafety behaviours, and biosafety documentation and training) [105].

A summary of the findings was prepared and the main findings were shared with the hospital management and laboratory staff. The data collection team paid a courtesy call to the hospital management and explained the purpose of the assessment. After that, the team visited the laboratory and interacted with laboratory staff regarding the purpose of their visit. The team toured the laboratory and reviewed documents including SOPs. The questionnaire was administered for two days (approximately eight hours per day) per facility by four data collectors, including two public health experts and two clinical microbiology experts. Since the facilities are sparsely distributed, data collection was done for 18 days, taking into consideration the travel days.

4.4. Data Analysis

The LAARC tool is a self-scoring tool; therefore, the data were entered into the LAARC tool for initial scoring based on each indicator. The minimum score was 0% and the maximum score was 100%. Low capacity to conduct basic medical bacteriology and test for AMR scored from 0-49%, moderate capacity was scored 50-79%, whereas good capacity was scored 80-100% [105]. All the charts were developed using Microsoft Excel version 2013. The overall scores for the hospitals were generated average was calculated to produce the overall capacity of the laboratory to conduct AMR surveillance. For the assessed indicators, the scores were aggregated for all hospitals and an average score was produced to indicate the capacity of laboratories to perform activities under that indicator. Scores of 0-49% meant that the laboratory needed significant improvement in conducting the activities under such indicators. Scores of 50-79% meant that some improvement was required, while scores of 80% and above were satisfactory.

5. Conclusions

This study demonstrates that the assessed hospitals had low capacity regarding testing and surveillance of AMR. The presence of a physical laboratory in all seven hospitals is very important to setting up and implementing AMR testing and surveillance. There is a need to strengthen all seven laboratories in the areas of laboratory conditions, equipment, LIS, data management, quality control, specimen collection and handling, pathogen identification methods, conducting of AST, and safety standards. These improvements could in turn improve diagnostic stewardship and patient outcomes. Additionally, this strategy can be extended to other laboratories across the country.