Koudokpon Et Al., 2024
Koudokpon Et Al., 2024
Strengthening clinical
OPEN ACCESS bacteriology laboratory
diagnostics to combat sepsis and
EDITED BY
Kordo Saeed,
Southampton General Hospital,
United Kingdom
REVIEWED BY
antimicrobial resistance in Benin:
Jane Cunningham,
Basingstoke and North Hampshire Hospital,
United Kingdom
a train-the-trainer approach
Andrew Rosser,
Southampton General Hospital, Hornel Koudokpon 1, Brice Boris Legba 1, Victorien Dougnon 1*,
United Kingdom
Sointu Mero 2,3, Honoré Bankole 1 and Kaisa Haukka 3,4
*CORRESPONDENCE
Victorien Dougnon 1
Research Unit in Applied Microbiology and Pharmacology of natural substances, Research
victorien.dougnon@gmail.com Laboratory in Applied Biology, Polytechnic School of Abomey-Calavi, University of Abomey-Calavi,
RECEIVED 18 September 2023 Abomey-Calavi, Benin, 2 Human Microbiome Research Program, Faculty of Medicine, University of
ACCEPTED 04 April 2024 Helsinki, Helsinki, Finland, 3 Physicians for Social Responsibility, Helsinki, Finland, 4 Department of
PUBLISHED 19 April 2024
Microbiology, University of Helsinki, Helsinki, Finland
CITATION
Koudokpon H, Legba BB, Dougnon V, Mero S, Introduction: Improved laboratory diagnostics is needed to support sepsis
Bankole H and Haukka K (2024)
Strengthening clinical bacteriology laboratory diagnosis and combat increasing antibiotic resistance in Benin. We trained
diagnostics to combat sepsis and clinical laboratory experts and technicians to improve their skills in accurate and
antimicrobial resistance in Benin: a train-the- up-to-date diagnostics.
trainer approach.
Front. Med. 11:1281418. Methods: A Train-the-Trainer (TtT) approach was used to design the course that
doi: 10.3389/fmed.2024.1281418 combines theoretical and practical laboratory skills, specifically addressing the
COPYRIGHT knowledge gaps we had previously identified in our national survey. Pedagogical
© 2024 Koudokpon, Legba, Dougnon, Mero,
methods were student-centered, including peer learning, use of online materials,
Bankole and Haukka. This is an open-access
article distributed under the terms of the practical laboratory work and pre-and post-course tests.
Creative Commons Attribution License
Results: We first trained 10 trainers who in turn trained 40 laboratory technicians
(CC BY). The use, distribution or reproduction
in other forums is permitted, provided the from across the country, from both public and private clinical and veterinary
original author(s) and the copyright owner(s) laboratories. The trainers also prepared standard operation procedures for blood
are credited and that the original publication
culture and antibiotic susceptibility testing based on international standards.
in this journal is cited, in accordance with
accepted academic practice. No use, Three months after the training, follow-up visits were made to the laboratories
distribution or reproduction is permitted where the implementation of the new skills was evaluated. The progress of the
which does not comply with these terms.
participants observed during the course and the implementation of the new
skills afterwards proved the training to be effective.
Discussion: The professional networks created during the training, the
empowerment that utilizes local knowledge resources, and the government
support for our initiative can be expected to bring sustainability to the
initiative and support the participation of Beninese laboratories in international
surveillance programs in the future.
KEYWORDS
1 Introduction
The clinical bacteriology laboratory plays a key role as a provider of diagnostic services for
quality patient care. Blood cultures and Antibiotic Susceptibility Testing (AST) help identify
the cause of sepsis and determine antimicrobial resistance (AMR) of the pathogens (1). Sepsis
is life-threatening organ dysfunction caused by a dysregulated host response to infection (2).
In 2017, 11 million deaths were reported to be sepsis-related, across the country to assess the training needs (14). The survey
accounting for approximately 20% of all global deaths (3). In 2019, the identified deficiencies in the knowledge and practices of laboratory
global impact of AMR was estimated to be 4.95 million deaths due to technicians regarding culturing blood samples, identifying pathogens
infections caused by resistant bacteria (4). Neonatal sepsis is the third causing sepsis and AST. The survey, along with additional visits to
leading cause of neonatal death worldwide, particularly in low-and selected hospitals in different parts of the country and all the
middle-income countries (LMICs), with many of the deaths attributed physicians interviewed, indicated dissatisfaction with the local
to AMR (5–8). Africa is the most affected continent where many laboratory services, the laboratory equipment used for AST, the
endogenous factors and the increasing prevalence of AMR complicate proficiency of the laboratory staff and reliability of the results. The
the treatment of sepsis (6, 9–11). Furthermore, reliable diagnostic laboratory technicians and managers as well as the hospital
laboratory testing is not readily accessible in sub-Saharan Africa, management strongly supported the planned training activities. The
leading to frequent misdiagnosis (10, 12, 13). Ministry for Health of Benin also endorsed our training activity,
A recent study by Legba et al. (14) in Benin reported that six which is crucial for ensuring the initiative’s sustainability.
laboratories in the country can perform blood cultures, while AST is The flowchart for the training is shown in Figure 1. To develop the
done in 23 laboratories. However, the number of tested samples (mainly course curriculum, eight experts consisting of Beninese and Finnish
urine, also some cervicovaginal secretion and blood culture samples) is laboratory and health professionals were involved in formulating the
very low due to inadequate infrastructure and cost to a patient. course objectives and methods. Four topics were chosen for the
Additionally, deficient skills of laboratory personnel lead to unreliable training: (1) blood culture; (2) bacterial identification techniques; (3)
test results. Therefore, nationally uniform training based on standardized AST; and (4) quality assurance in laboratory.
techniques is needed to improve the accuracy of laboratory diagnostics
(12, 15). Reliable test results are essential for both targeted treatment of
patients and empiric treatment when the prevalent AMR characteristics 2.2 Recruitment of the trainers and trainees
of the sepsis-causing organisms are known in the region (14).
To improve the quality of sepsis diagnostics and AST in all regions Ten trainers to enroll were identified based on their academic
of Benin, we adopted a Train-the-Trainer (TtT) approach to train qualifications. They were medical microbiologists holding at least a
several laboratory professionals in a short time and ensure sustainable Master’s degree and a position as a senior technician in a hospital
transfer of new skills. TtT is a training methodology where individuals, bacteriological laboratory or they were involved in University
experienced in a particular subject or skill, undergo training to become training in medical microbiology as teachers or PhD students.
trainers themselves. The goal is to empower these individuals to deliver Further 40 technicians selected as trainees included 25 technicians
the same training to others, creating a cascading effect of knowledge from the laboratories carrying out bacteriological examinations
dissemination (16). The TtT approach has been successful in similar including AST. Further 13 technicians were chosen from among
continuous professional training initiatives in LMICs (17–20). In our laboratory technicians working at the universities as research
Beninese setting, the TtT approach was considered new and innovative, laboratory technicians. Benin has only two veterinary laboratories,
since primarily instructor-centered teaching methods, such as lecturing and both were asked to send a laboratory technician to the course,
to large classes, are used and resources for hands-on laboratory training which they did. Of the 40 technicians participating the training, 22
are scarce. The traditional approach does not provide the kind of skills were males and 18 females. Twenty-four technicians were aged 20–30
that technicians need in their work, nor does it allow for monitoring and 16 aged 31–50.
the practical application of the concepts learned in training. Therefore,
we chose methods that encourage peer-learning to enable experienced
technicians to both update their skills and to pass on their knowledge 2.3 Course development as a way to train
to others, without compromising the quality of teaching. the trainers
Our training initiative was aligned with the governmental goal to
improve laboratory functioning and reliability in Benin (21). The Beninese In developing the training course, a learner-centered participatory
national action plan against Antimicrobial Resistance (PAN-RAM – Bénin method was used, with trainers and experts collaboratively designing
2019–2024), strategic axis 2 (Surveillance, laboratory capacity and research the content and materials. The three-week TtT course included
on AMR) provides guidelines for the continuous training of laboratory individual and group study, discussions, laboratory practice and
personnel working in microbiological laboratories (Action 2.2.1.1) and exchange of best practices among participants. Through sessions of
networking of laboratories for the quality approach. Accordingly, the meticulous discussions to reach consensus, they also created a
objective of our training was to build a network of trainers with good skills comprehensive guide for a new five-day course. This guide includes
and capable of training more laboratory technicians to improve the quality 21 standard operating procedures (SOPs) for bacteriological
of clinical bacteriology laboratory diagnostics in Benin. laboratories, aligned with WHO guidelines but adapted to local
conditions and validated by Beninese and Finnish clinical
microbiology professionals.
2 Methods, implementation, and
results
2.4 Structure for the five-day training
2.1 Identification of the training needs course
Before starting the training activities, a survey was conducted The course for the trainees covered four topics over 5 days (40 h),
using face-to-face interviews with laboratory staff and physicians followed by a shorter sixth day dedicated to the final assessments and
FIGURE 1
Flow chart of the training course.
closing ceremony. The topics were, Days 1 and 2: conducting a blood pedagogical principal as it promotes learner engagement, reflective
culture using manual method, following instructions of WHO practice, critical thinking, and skills development.
Laboratory Manual for the Examination and Processing of Human The specific pedagogical techniques we applied included:
Blood, Day 3: Bacterial identification using API and biochemical tests Pre-assignments. A few months before the training, the
for Staphylococcus aureus identification, Day 4: conducting AST using participants were requested to follow the Massive Open Online
disk diffusion method following the EUCAST guidelines, Day 5: Courses (MOOCs) listed in Table 2. At the beginning of the training,
internal and external quality assurance in bacteriological laboratory the themes of the online courses were discussed with the participants,
according to the WHO recommendations. Each day was structured allowing us to assess what they had learnt.
to contain introduction to the topic by the trainers, independent Peer learning. Pairing a more experienced and a more novice
work, group work, practical laboratory work and recapping the technician to work together in the laboratory and during various fact-
learned contents together with the trainers. The detailed program for finding activities created an opportunity to pass on practical
the training is shown in Table 1. Altogether 40 trainees participated experience and to develop the teaching skills of the trainers
in the three training courses, each including 13–14 technicians. and trainees.
Utilizing freely available online audiovisual and reading
materials. The trainers/trainees searched information from sources
2.5 Learning philosophy and teaching such the YouTube videos produced by reliable authorities in specific
approaches topics. Some websites were indicated by the experts, but the trainers
and trainees were also encouraged to search for new sites, e.g., the
In planning the pedagogical approach, we were inspired by the major French universities and hospitals provide suitable material in
principal of the constructivist learning theory: Constructivism implies French. For future sustainable continuous independent learning, it
that learners are encouraged to construct their own knowledge instead was important for the trainers and trainees to get familiar with using
of copying it from an authority, be it a book or a teacher, in realistic freely available up-to-date material, since the instructions available in
situations instead of decontextualized, formal situations such as the Beninese clinical laboratories are often outdated and the chances
propagated in traditional textbooks, and together with others instead to participate in professional further education are rare. Materials
of on their own (22, 23). The TtT approach aligns well with this utilized on the course are listed in Table 2.
TABLE 1 Topics covered by the training course, detailed contents, and examples of implementation.
Bacterial identification (Day 3) • Microscopic observation and gram-staining Searching for information on biochemical tests for
• Choice of solid culture media bacterial identification, assessing the results.
• Preparation of culture media Conducting the API 20E test in practice
• Seeding techniques
• Description of colonies and other cultural characteristics of bacteria
• Biochemical identification
Conducting antibiotic susceptibility • Different methods for performing AST Searching for information and discussing different
testing (AST) (Day 4) • Criteria for choosing the antibiotics to be tested ways to carry out AST, preparation of the
• Incubation conditions (temperature, duration) inoculum, techniques of inoculation, sharing of
• Interpretation of the results of the AST experience between professionals. Conducting the
• Identification of ESBLs: microbiological and biochemical techniques laboratory work by the trainees
• Quality control
• Study of the EUCAST guidelines
Quality assurance in bacteriological • Quality criteria Clarification of the concept of quality assurance in
laboratory (Day 5) • Internal quality control microbiology, conducting quality control on
• External quality assessment culture media, antibiotic disks and sterility and
• Maintenance of the laboratory equipment fertility testing of culture media
• Quality control of laboratory reagents, culture media, antibiotic disks
TABLE 2 Online material indicated to the participants before and during the training.
Laboratory work. The 5-day training course took place primarily other under the guidance of a qualified nurse. The blood samples
in the laboratory allowing the trainees to put in practice what they were spiked with Escherichia coli, Klebsiella pneumoniae, Salmonella
had learnt, for example from the YouTube videos. This was spp., Staphylococcus aureus or a mixture of E. coli and S. aureus by the
exceptional in the resource-poor settings, where the financing is instructors, without the course participants knowing the identity of
seldom enough for providing all the learners an opportunity to the bacteria. During the training the participants practiced
hands-on experimentation. In addition, some role-play components identifying the bacteria in their own samples and conducting AST
were included, such as the pairs taking a blood sample from each to them.
TABLE 3 The average pre-test and post-test scores for each group (maximum score 20).
Post test Post-test score (mean ± SD) 14.5 ± 1.6 15.3 ± 1.6 14.0 ± 1.7 14.7 ± 3.1
p-value 0.0012
2.6 Evaluation of the training results and logistics, atmosphere, time management and the competence of the
methods trainers. In the open feedback, the innovative teaching approach and
small group sizes were particularly appreciated, because they allowed
2.6.1 On-site assessment by pre-and post-tests adjustments to course structure and individualized support. The
At the beginning of the onsite training, the participants’ trainers, in turn, expressed their satisfaction with the high motivation
knowledge and skills on the training topics were assessed by pre-tests of the participants, the benefits of the new teaching approach and the
including both theoretical questions and practical laboratory tasks encouraging working environment created by small group sizes. They
(Supplementary appendix 1). The theoretical part of the test included recommended frequent offering of similar courses. In the future,
open questions on the concept of sepsis, indicators for blood culture including new bacterial species (e.g., Haemophilus influenzae and
contamination, identification of typical bacteria infecting blood, Streptococcus spp.) was considered to be important as well as allocating
choosing antibiotics for AST and quality control. For the practical part even more time for practical exercises.
in the laboratory, each participant was given a sample containing
E. coli, S. aureus, both, or neither in Müller-Hinton broth. The 2.6.3 Post-training on-site monitoring
participant, not knowing the bacterial content of the broth tube, The trainees were expected to apply and communicate the newly
carried out the macroscopic and microscopic examination of the acquired knowledge in their home laboratories and to train their
sample, chose the appropriate solid culture medium and carried out colleagues. Three months after the course, an on-site evaluation was
the inoculation. carried out by visiting 15 of the laboratories to assess the improvements
The pre-test assessment allowed some last-minute adjustments in to the daily practice after the training. The evaluation was carried out
the course contents to meet the specific knowledge gaps of the in the actual work situation and lasted 4 h in each laboratory. We had
participants. It also served as self-assessment for the trainees. The previously collected baseline information from the laboratories (14),
pre-and post-tests were identical allowing us to evaluate the which allowed us to assess the positive changes in the practices related
improvement in the participants’ knowledge and skills during the to external and internal quality assurance, a blood culture, bacterial
course and efficacy of the training. To measure the progress, identification methods and AST. During the visits, the evaluators
we compared participants’ test results before and after the training noticed that the new SOPs produced by the trainers were in effective
(Table 3). The average improvement of the test score was 4.5 and the use. However, shortcomings were detected, for example, in sample
p-value 0.001 indicating indicated a significant difference between the handling and storage, storage of quality control strains and
scores obtained by the participants before and after the training. interpretation of AST results and the technicians were advised for
All the pairs were also asked to produce a course report that necessary corrections. Consequently, managers of the health
summarized the practical work carried out, including the establishments (physicians in most cases) expressed their satisfaction
methodology and the results obtained. This allowed the instructors to to the training results.
evaluate the pair-work and learning outcomes. The participants were
also asked to list the three most important concepts or skills that they
had learned during the training. The answers included items such as: 3 Discussion
taking a blood sample for a blood culture, interpreting the API20E
results, conducting, interpreting, and controlling the quality of AST, We designed and implemented a Train-the-Trainer initiative
phenotypic techniques for bacterial identification, familiarization with aimed at improving the quality of clinical bacteriology laboratory
the latest version of EUCAST breakpoints set by the European diagnostics for bacteria causing sepsis and AST. We first trained 10
Committee on Antimicrobial Susceptibility Testing. laboratory professionals to be trainers, who then carried out training
of 40 trainees, who were laboratory technicians from different parts of
2.6.2 Feedback on the training by the trainees Benin. The TtT approach was chosen, since it is suited for short
and trainers continuous professional training needs, can combine expertise of
Feedback forms completed by participants at the end of the international and local experts, can be completed in a short time,
training showed unanimous approval of the teaching methods, with creates a cascade of knowledge transfer and is scalable. Our training
excellent or very good ratings (Supplementary appendix 2). improved the skills of the Beninese laboratory technicians. They can
Participants were also satisfied with the organization of the training, provide more reliable information for effective treatment of patients
and data for monitoring pathogens causing blood infections and their participate the training, but due to the travel restrictions caused the
AMR profile. We were able to promote standardization of the Covid19 epidemic, the training was organized utilizing local expertise
laboratory testing techniques in Benin by inviting participants from in Benin, with the foreign experts mainly commenting the written
different regions and sharing with them the SOPs drafted jointly by plans for training and giving some online support. The new approach
the experts and trainers. By basing the SOPs on the WHO was saluted with enthusiasm among the Beninese professionals and
recommendations, our purpose is to enhance reporting of the many previously hidden skill resources were successfully tapped. The
Beninese laboratory results to international surveillance systems such approach based on the active participation of local experts to guide
as the Global Antimicrobial Resistance and Use Surveillance System continuous education and to encourage methods that actively engage
(GLASS). trainers and trainees was new in Benin. It turned out to be very
The central government has previously run some training courses successful and empowered the local healthcare experts and
for clinical bacteriology laboratories, but ours were the first to involve laboratory professionals.
both the private and public laboratories to harmonize the national
practices in line with the international standards. The national strategy
for fighting AMR emphasizes the One Health approach (21), but in 4 Conclusion
practice the laboratory services for the animal and environmental
samples are even more lacking than for the human samples. Also, the The Train-the-Trainer approach was shown to be an effective way
One Health aspect was considered by including technicians from the to enhance the skills of laboratory professionals. Our training initiative
only two veterinary laboratories in Benin into the training activities. combined theoretical and practical learning to improve the skills and
We included in the training technicians from both clinical and to correct knowledge gaps identified during a national survey. It
veterinary laboratories to enhance adopting similar laboratory enabled experienced technicians to not only update their skills in
techniques for human, animal and environmental samples and practices related to blood culture and AST, but also to network and
consequently allowing, for example, easier tracing of infection sources. share their knowledge with others, promoting sustainable transmission
Typically, access to continuous training is restricted in LMICs, and of the new skills. Course training was combined with the development
factors such as the poor fit between existing learning activities and the of standardized SOPs adapted to local conditions. The SOPs were
desire of participants for practical learning, and uninspiring teachers implemented in local laboratories with the help of the trainees, and
can reduce motivation to attend available training (24). Our their use was examined during follow-up visits to the laboratories.
interactive, learner-centered methods were able to circumvent these This will contribute to improve the accuracy and reliability of
problems. Feedback discussions during training of the trainers showed diagnostic test results in the clinical bacteriology laboratories in
clearly that networking with colleagues and writing the SOPs were Benin. Our training initiative represents a successful strategy for
seen to be very empowering to the participants. Many laboratory strengthening laboratory capacity in resource-limited settings. The
professionals, especially the senior ones, who have collected plenty of recommendations arising from the training, such as extending
valuable silent knowledge during their career, stated that this was the training to a larger number of laboratory professionals, will be duly
first time they were heard as real experts in laboratory diagnostics. considered for inclusion in future projects.
They considered keeping up the newly formed collegial network as
important way to share up-to-date knowledge and concerns also in
the future. Together they can also have a stronger influence in Data availability statement
planning the laboratory diagnostic practices in the hospitals.
We monitored the impact of training by making follow-up visits The original contributions presented in the study are included in
to the laboratories. Ideally the visits would be repeated after some the article/Supplementary material, further inquiries can be directed
time, for example half a year after the training, to ensure the positive to the corresponding author.
long-term effects of the training. Changes such as job transfers can
compromise the gains of the training and for sustainable improvement,
it is essential to organize the training courses in regular bases so that Author contributions
more staff from each laboratory would have access to them. Also
formalizing the peer-mentoring as part of a formal apprenticeship HK: Conceptualization, Formal analysis, Investigation,
program for new laboratory technicians would be a way to perpetuate Methodology, Project administration, Resources, Supervision,
the achievements. The course can also serve as a basis for the Validation, Visualization, Writing – original draft, Writing – review &
development of a more elaborate continuing education program editing. BBL: Conceptualization, Formal analysis, Funding acquisition,
supported by the Ministry of Health. Investigation, Methodology, Project administration, Resources,
In this communication, we have highlighted the pedagogical Supervision, Validation, Visualization, Writing – original draft,
choices made, the objectives achieved, and the feedback from the Writing – review & editing. VD: Conceptualization, Formal analysis,
participants to our bacteriology laboratory diagnostics training. Funding acquisition, Investigation, Methodology, Project
We hope that our experience can serve as a model that inspires the administration, Resources, Supervision, Validation, Visualization,
creation of more TtT activities for continuous training of professionals Writing – original draft, Writing – review & editing. SM:
in various fields in Benin and beyond. For sustainability of the activity, Conceptualization, Methodology, Project administration, Validation,
the continuous endorsement by the local Ministry of Health or Visualization, Writing – original draft, Writing – review & editing.
another relevant ministry is needed. In our case, the initial plan HB: Methodology, Writing – original draft, Writing – review &
involved the presence of Finnish clinical laboratory experts to editing. KH: Conceptualization, Formal analysis, Funding acquisition,
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