Microbial Contamination of Herbal Medicines in Africa,2000-2024: A Systematic Review

Abstract

Introduction:

Herbal medicine has been a cornerstone of healthcare for centuries, with an estimated 80% of the world’s population relying on it. In Africa, herbal medicine is the backbone of rural healthcare, serving 80% to 90% of the population. Despite its widespread use, the safety of herbal medicine raises a significant concern considering the lack of regulation and testing, particularly in Africa. Microbial contamination is a primary safety risk threatening consumer health. In this systematic review, we aimed to synthesise evidence on microbial contamination in herbal medicines across Africa, provide a clear understanding of the problem, and inform effective public health interventions regarding microbial contamination of herbal medicines in Africa.

Method:

The systematic review was conducted in accordance with the PRISMA guidelines. A literature search was conducted across PubMed, Web of Science, Science Direct, Scopus, and Google Scholar using appropriate search terms. Eligible studies were selected based on predetermined criteria, and data were extracted and analysed.

Results:

The review included fifty eligible studies in Africa, with a combined sample size of 1996, of which 1791 showed microbial contamination. Bacterial contaminants were reported in 98% of studies, with Escherichia coli (62%) being the most reported bacteria, followed by Staphylococcus aureus (57%), and Bacillus spp. (55%). Fungal contaminants were reported in 70% of studies, with Aspergillus spp. (40%) being the most reported, followed by Penicillium spp. (27%) and Candida spp. (26%). Parasitic contaminants were reported in 2% of the studies reviewed. A total of 70 bacterial species, 37 fungal species, and 6 parasite species were identified in this review.

Conclusion:

Herbal medicines in Africa pose significant health threats to consumers due to the high prevalence of diverse microbial contaminants and clinically significant pathogens. This emphasises the need for stricter regulations and quality control measures in the production, sale and use of herbal medicines.

Keywords

Herbal medicine herbal medicine safety herbal products microbial contamination safety assessment Africa medicinal plants public health

Introduction

Herbal medicine has been an integral resource for health in communities globally for centuries. It is estimated that 80% of the world’s population use herbal medicines.^1
-4 In Africa, herbal medicine is the backbone of rural healthcare, providing essential support to a significant number of the population (an estimated 80%-90%).⁵ The patronage and use of herbal medicines have increased due to their availability, accessibility, and affordability.^6
-8 They provide a practical alternative to healthcare services in the rural communities of developing nations.⁹

Considering the expanding market for herbal remedies across African countries, it is important to address all safety concerns associated with their use.¹⁰ Several herbal products used in Africa remain untested and unregulated,^1,4,11,12 posing significant health risks to consumers. According to a survey conducted by the World Health Organisation (WHO), only 43% of African member states currently have regulations in place for herbal medicines.⁴ The lack of effective regulation and monitoring make consumers vulnerable to diseases.¹³ Typically, the safety risks associated with herbal medicines include contamination by microbiological agents (such as bacteria and fungi), and chemical agents (such as metals, pesticides, residual solvents, and mycotoxins).¹⁴ Microbial agents are however, the most implicated contaminants in herbal medicines.^11,12,15 The presence of pathogenic microbial contaminants in herbal medicines has generated increased apprehension, as they can lead to the development of serious infections.¹⁶

Across Africa, research on the microbial safety of herbal medicines is only largely conducted within individual countries. Thus, the fragmented nature of the relevant research hinders the development of continent–wide, comprehensive herbal safety guidelines and public health policies. It is therefore important to curate evidence that reflects the extent and diversity of microbial contamination in herbal medicines throughout the African region. To the best of our knowledge, no published review specifically collates and synthesises the evidence on microbial contamination in herbal medicines across Africa. While a previous review by Opuni et al.¹⁵ examined various contaminants in herbal medicines across low– and middle–income countries, it did not address parasitic contaminants, limiting our understanding of the full spectrum of microbial risks associated with herbal medicines. Similarly, the review by Walusansa et al.¹² only examined bacterial contaminants in herbal medicines from East Africa, overlooking other microbial contaminants. Our systematic review aimed to provide a holistic and up–to–date analysis of the microbial contaminations associated with herbal medicines in Africa, integrating findings that have emerged since the publication of previous reviews. This study assessed original research articles that explored the presence and diversity of microbial contaminants in herbal medicines across African countries, spanning from 2000 to 2024. By examining this body of research, we sought to identify emerging trends and challenges concerning microbial contamination in herbal medicines in the 21st century. This knowledge is necessary to guide the development of relevant public health interventions and offer direction for future research on herbal medicine safety in Africa.

Method

Search strategy

This systematic review was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta–Analyses (PRISMA) guidelines.¹⁷ Literature search was conducted between June 7th and 15th, 2024, across PubMed, Web of Science, Scopus, Science Direct, and Google Scholar, to identify articles related to the microbial contamination of herbal medicines in Africa, from year 2000 to 2024. The primary search strategy incorporated both Medical Subject Headings (MeSH terms) and keywords such as ‘Herbal Medicine’[Mesh] OR herbs OR ‘Plant medicine’ OR ‘Plants, Medicinal’[Mesh] OR ‘Plant Preparations’[Mesh] AND ‘Microbiology’[Mesh] OR microbes OR ‘Bacteria’[Mesh] OR ‘Fungi’[Mesh] OR ‘Viruses’[Mesh] OR ‘Colony Count, Microbial’[Mesh] AND ‘Africa’[Mesh]. The citations and references of the identified articles were carefully reviewed to include all relevant studies. The full electronic search strategy for all the databases used is shown in Supplemental Table 1.

Eligibility criteria

The review exclusively examined studies conducted from 2000 to 2024, which presented evidence of microbial contamination in herbal medicines across Africa. These studies were required to identify the specific microbial contaminants isolated from herbal medicines and determine the prevalence and/or load of these microbes. To ensure the reliability of the findings, only peer-reviewed articles that employed standardised laboratory methods for assessing microbial contamination and were published in English were included. Studies that investigated contaminants and adulterants other than microbes were excluded. Additionally, studies conducted outside Africa, review articles, and studies that did not specify microbial contaminants or provide sufficient information on contamination levels in herbal medicines were excluded from the review.

Study selection

The selection of studies for this review involved a three–phase screening process to retrieve articles of interest. In the initial phase, duplicates were identified and manually eliminated using the systematic review tool ‘Rayyan QCRI’.¹⁸ Two researchers then independently screened the remaining articles by reading the titles, abstracts, and keywords to identify relevant studies. Finally, the full texts of the remaining articles after the second screening phase were thoroughly reviewed to determine which studies met the inclusion criteria and were ultimately included in the review. The PRISMA flow diagram below (Figure 1) illustrates the article selection process.

Figure 1.

PRISMA flow diagram providing a detailed representation of the article selection process.

Quality assessment

To evaluate the quality of the included articles, we employed the modified Oxman and Guyatt score,¹⁹ an analytical tool adapted from previous systematic reviews on herbal medicines.^15,20,21 This tool assessed the study methodology, country of origin, and specific microbial contaminants reported, with 1 point allocated per dimension for a maximum score of 10. Two authors independently assessed and scored the articles, and discrepancies were resolved through consensus among all 3 authors. Articles with total scores ranging from 8 to 10 were considered to be of good quality, those scoring from 5 to 7 as fair, and those scoring from 0 to 4 as poor quality. The scoring system for quality appraisal and the assessment of included studies are presented in Supplemental Tables 2 and 3, respectively.

Data extraction and analysis

Two independent researchers extracted data from 50 articles that met the inclusion criteria. Each researcher entered the extracted data into spreadsheets, documenting various attributes, including author(s) name, year of publication, country, sample size, number of contaminated samples, identification methods, type of microbial contaminant, microbial loads, and specific microbial contaminants isolated. The geographical distribution of the included articles was visualised using a map, while bar charts and tables were used to visualise the distribution of study characteristics and findings. Bar graphs illustrating microbial contaminants and their occurrence levels in the included studies were created using Microsoft Excel. The data for these graphs were sourced from the individual studies included in this review.

Results

From an initial pool of 8005 search results, 50 research articles were selected for inclusion after the three–phase screening process. The quality of the selected articles ranged from fair to good based on the quality assessment parameters used.

Characteristics of the eligible studies

Table 1 shows a summary of the characteristics of the 50 studies included in this review. The highest number of eligible studies came from Nigeria, 25 (50%), followed by Ghana with 9 (18%), Kenya with 4 (8%), South Africa with 3 (6%), and Tanzania with 2 (4%). Côte d’Ivoire, Malawi, Cameroon, Sierra Leone, Benin, Uganda, and Lesotho, contributed 1 study each (2%). The distribution of these studies across different regions is shown in Figure 2.

Table 1.

Characteristics of the included studies in this review.

Reference	Year	Country	Sample size	Samples contaminated	Identification technique	Microbial load		Contaminant group	Specific organisms isolated
Reference	Year	Country	Sample size	Samples contaminated	Identification technique	Bacterial load	Fungal load	Contaminant group	Specific organisms isolated
Hassan et al.²²	2021	Kenya	86	72	Conventional culture method	NA	NA	Bacterial	Escherichia coli Salmonella typhi Salmonella paratyphi Enterobacteriaceae
Abba et al.²³	2009	Nigeria	150	131	Conventional culture method	0 to 2.25 × 10⁸ cfu/mL	NA	Bacterial	Salmonella typhi Shigella spp. Escherichia coli Staphylococcus aureus
Archibong et al.²⁴	2017	Nigeria	60	57	Conventional culture method	Registered samples 1.2 × 10³ cfu/mL to 2.1 × 10⁶ cfu/mL Unregistered samples 3.6 × 10³ cfu/mL to 2.42 × 10⁸ cfu/mL	Registered samples 1.0 × 10² cfu/mL to 1.4 × 10⁵ cfu/mL Unregistered samples 2.0 × 10² cfu/mL to 2.0 × 10⁶ cfu/mL	Bacterial Fungal	Providencia rettgeri Enterobacter asburiae Acinetobacter baumannii Escherichia coli Bacillus spp. Staphylococcus spp. Candida albicans Candida krusei Scedosporium aurantiacum Penicillium marneffei Aspergillus niger Phaeoacremonium parasiticum
Brooks and Takim²⁵	2014	Nigeria	28	20	Conventional culture method	Solid samples 2.05 × 10⁴ cfu/g to 5.6 × 10⁴ cfu/g Liquid samples 3.8 × 10⁴ cfu/mL to 6.8 × 10⁴ cfu/mL	NA	Bacterial Fungal	Salmonella spp. Escherichia coli Staphylococcus aureus Pseudomonas aeruginosa Bacillus subtilis Klebsiella spp. Enterobacter spp. Aspergillus flavus Aspergillus niger Rhizopus spp. Mucor spp. Fusarium spp. Candida tropicalis
Govender et al.²⁶	2006	South Africa	15	15	Conventional culture method	1.2 × 10³ cfu/mL or g to 1.19 × 10⁹ cfu/mL or g	0 to 2.5 × 10⁶ cfu/mL	Bacterial Fungal	Bacillus spp. Pantoea spp. Rahnella aquatilis Acinetobacter baumannii Pseudomonas spp. Chryseomonas spp. Flavimonas spp. Stenotrophomonas maltophilia Ewingella americana Salmonella spp. Klebsiella pneumoniae Bordetella spp. Pasteurella pneumolytica Serratia spp. Penicillium spp. Mucor spp. Aspergillus spp
Mautsoe et al.²⁷	2021	Lesotho	5	5	Conventional culture method	5.6 × 10⁴ cfu/mL to 3.6 × 10⁸ cfu/mL	3.0 × 10⁵ cfu/mL to 6.0 × 10⁸ cfu/mL	Bacterial Fungal	Pseudomonas aeruginosa Coliforms Yeast and moulds
Nwankwo and Olime²⁸	2019	Nigeria	60	60	Conventional culture method	Liquid 3.10 × 10² cfu/mL to 2.56 × 10³ cfu/mL Powder 9.0 × 10¹ cfu/g to 1.5 × 10² cfu/mL	Liquid 2.0 × 10¹ cfu/mL to 1.9 × 10² cfu/mL Powder 1.0 × 10¹ cfu/mL to 1.0 × 10² cfu/mL	Bacterial Fungal	Bacillus spp. Bacillus subtilis Bacillus polymyxa Bacillus cereus Bacillus licheniformis Aspergillus spp. Penicillium spp.
Odonkor et al.²⁹	2011	Ghana	10	8	Conventional culture method	2.2 × 10³ cfu/mL to 6.2 × 10³ cfu/mL	6.2 × 10³ cfu/mL	Bacterial Fungal	Staphylococcus aureus Pseudomonas aeruginosa Bacillus spp. Fungi
Kalumbi et al.³⁰	2020	Malawi	29	20	Conventional culture method	NA	NA	Bacterial	Citrobacter spp. Bacillus spp. Coagulase negative Staphylococcus Klebsiella spp. Enterobacter spp.
Walusansa et al.³¹	2022	Uganda	140	140	Conventional culture method	Liquid 0.0 to 1.42 × 10⁷ cfu/mL Solid 1.8 ×10³ cfu/g to 1.67 ×10⁷ cfu/g	NA	Bacterial	Klebsiella pneumoniae Escherichia coli Staphylococcus aureus Klebsiella oxytoca Bacillus cereus Pseudomonas aeruginosa Enterobacter spp.
Ezekwesili-ofili et al.³²	2014	Nigeria	210	210	Conventional culture method	NA	NA	Bacterial Fungal	Escherichia coli (EPEC, EHEC) Bacillus spp. Salmonella spp. Enterococcus faecalis Pseudomonas spp. Klebsiella spp. Aeromonas spp. Coliforms Aspergillus flavus Cladosporium spp. Rhizopus spp. Penicillium spp. Mucor spp. Aspergillus niger Curvularia spp. Candida spp. Geotrichum spp. Aspergillus fumigatus
Tatfeng et al.³³	2010	Nigeria	6	6	Conventional culture method	0.2 × 10² cfu/mL to 4.7 × 10⁷ cfu/mL	0.2 × 10² cfu/mL to 4.7 × 10⁷ cfu/mL	Bacterial Fungal	Enterococcus faecalis Staphylococcus aureus Escherichia coli Bacillus spp. Staphylococcus epidermidis Pseudomonas aeruginosa Proteus mirabilis Mucor spp. Serratia marcescens Aspergillus niger
Walther et al.³⁴	2016	Tanzania	109	89	Conventional culture method	10² to 10⁴ cfu/mL	NA	Bacterial	Klebsiella pneumonia Enterobacter aerogenes
Kaume et al.³⁵	2012	Kenya	24	24	Conventional culture method	APC counts 1.5 × 10¹ cfu/g to 7.1 ×10⁸ cfu/g	<10 cfu/g to 9.0 × 10⁴ cfu/g	Bacterial Fungal	Coliforms Escherichia coli Staphylococcus aureus Yeast Mould
Van-Vuuren et al.⁸	2014	South Africa	75	75	Conventional culture method	3.03 × 10⁴ cfu/g to 4.22 × 10⁵ cfu/g	NA	Bacterial	Acinetobacter baumannii Acinetobacter lwoffii Bacillus amyloliquefaciens Bacillus lentus Bacillus megaterium Bacillus subtilis Bacillus vallismortis Enterobacter cloacae Klebsiella oxytoca Leclercia adecarboxylata Pantoea spp. Pseudomonas oryzihabitans Sphingomonas paucimobilis Streptococcus mitis Staphylococcus hominis
Igbeneghu and Lamikanra³⁶	2016	Nigeria	50	49	Conventional culture method	0 to 2.94 × 10¹² cfu/mL	0 to 3.54 × 10¹² cfu/mL	Bacterial Fungal	Bacillus cereus Citrobacter spp. Enterobacter spp. Escherichia coli Klebsiella spp. Pantoea agglomerans Proteus spp. Pseudomonas fluorescens Pseudomonas spp. Salmonella spp. Staphylococcus spp.
Kanu et al.³⁷	2015	Sierra Leone	20	20	Conventional culture method	30 cfu /mL to 9.37 × 10⁹ cfu/mL	30 cfu/mL to 1.60 × 10⁹ cfu/mL	Bacterial Fungal	Staphylococcus aureus Bacillus spp. Escherichia coli Staphylococcus epidermidis Salmonella spp. Candida albicans Aspergillus flavus Aspergillus niger Cryptococcus neoformans Trichoderma harzanium Aspergillus nidulans
Darkwah et al.¹⁰	2022	Ghana	30	30	Conventional culture method	Coliform count 3.1 × 10¹ cfu/mL to 1.7 × 10⁵ cfu/mL	NA	Bacterial Fungal	Escherichia coli Pseudomonas aeruginosa Bacillus spp. Citrobacter divergens Citrobacter spp. Staphylococcus aureus Staphylococcus spp. Enterobacter spp. Shigella sonnei Moraxella catarrhalis Serratia marcescens Candida spp.
Oladosu et al.³⁸	2020	Nigeria	20	10	Conventional culture method	Liquid 7.22 × 10⁴ cfu/mL Powder 1.35 × 10⁴ cfu/mL to 2.53 × 10⁴ cfu/mL	NA	Bacterial Fungal	Bacillus subtilis Shigella spp. Klebsiella pneumoniae Staphylococcus aureus Proteus spp. Pseudomonas aeruginosa Enterococcus feacalis Escherichia coli Alterneria spp. Aspergillus niger Aspergillus flavus Aspergillus fumigatus Cladosporium cladosporioides Mucor spp. Rhizopus arrhizus
Anie et al.³⁹	2022	Nigeria	7	7	Conventional culture method	1.8×10⁶ cfu/mL to 7.5 × 10⁶ cfu/mL	NA	Bacterial Fungal	Staphylococcus aureus Proteus spp. Pseudomonas spp. Streptococcus spp. Candida spp. Aspergillus niger Aspergillus flavus
Ideh and Ogunkunle⁴⁰	2019	Nigeria	12	10	Conventional culture method	1.0 × 10⁵ cfu/mL to 1.34 × 10⁷ cfu/mL	1.0 × 10⁵ cfu/mL to 1.5 × 10⁷ cfu/mL	Bacterial Fungal	Streptococcus spp. Staphylococcus spp. Salmonella spp. Enterobacteria Yeasts Moulds
Oshoma and Dijeh⁴¹	2017	Nigeria	10	10	Conventional culture method	9.5 × 10³ cfu/mL to 2.9 × 10⁴ cfu/mL	6.0 × 10³ cfu/mL to 1.8 × 10⁴ cfu/mL	Bacterial Fungal	Bacillus licheniforms Bacillus subtilis Pseudomonas aeruginosa Escherichia coli Staphylococcus aureus Staphylococcus epidermidis Penicillium spp. Aspergillus flavus Aspergillus niger Rhizopus spp. Mucor spp.
Turkson et al.⁴²	2020	Ghana	4	4	Conventional culture method	1.21 × 10³ cfu/mL to 2.23 × 10³ cfu/mL	1.01 × 10³ cfu/mL to 2.43 × 10³ cfu/mL	Bacterial Fungal	Aerobic bacteria Yeasts and moulds
Chinakwe et al.⁴³	2023	Nigeria	30	30	Conventional culture method	1.0 × 10⁶ cfu/mL to 7.8 × 10⁷ cfu/mL	3.0 × 10³ cfu/mL to 1.3 × 10⁸ cfu/mL	Bacterial Fungal	Bacillus spp. Corynebacterium spp. Micrococcus spp. Enterococcus spp. Staphylococcus spp. Mucor spp. Saccharomyces spp. Penicillium spp.
Abubakar et al.⁴⁴	2018	Nigeria	8	8	Conventional culture method	1.0 × 10⁷ cfu/mL to 1.8 × 10⁸ cfu/mL	NA	Bacterial	Staphylococcus aureus Escherichia coli
Osei-Adjei et al.⁴⁵	2013	Ghana	16	16	Conventional culture method	1.0 × 10² cfu/mL to 1.0 × 10⁹ cfu/mL	3.2 × 10⁵ cfu/mL	Bacterial Fungal	Bacillus subtilis Bacillus coagulans Bacillus licheniforms Enterobacter aerogenes Klebsiella oxytoca Serratia odorifera Cladosporium herbarum. Penicillium digitatum Aspergillus ustus Aspergillus oryzae Aspergillus sulphureus, Mycelia sterilia Trichosporon mucoides Saccharomyces kluyverii Rhodotorulla minuta Candida membranifasciens Sporobolomyces salmonicolor
Ampofo et al.⁴⁶	2012	Ghana	31	26	Conventional culture method	9.4 × 10 cfu/mL to 2.32 × 10³ cfu/mL	NA	Bacterial Fungal	Clostridium spp. Pseudomonas spp. Bacillus spp. Salmonella spp. Faecal coliform Heterotrophic bacteria Mould
Akande et al.⁴⁷	2013	Nigeria	15	15	Conventional culture method	1.0 × 10⁰ cfu/mL to 9.0 × 10⁵ cfu/mL	1.0 × 10⁰ cfu/mL to 8.0 × 10⁵ cfu/mL	Bacterial Fungal	Escherichia coli Salmonella spp. Klebsiella spp. Moraxella spp. Enterococcus spp. Pseudomonas spp. Bacillus spp. Staphylococcus spp. Streptococcus pneumoniae Alternaria spp. Rhizopus spp. Fusarium spp. Penicillium spp. Mucor spp. Candida spp.
Famewo et al.⁴⁸	2016	South Africa	9	9	Molecular technique	NA	NA	Bacterial	Raoultella ornithinolytica Rahnella aquatilis, Bacillus anthracis Bacillus cereus Salmonella enteric Enterobacter cloacae Klebsiella oxytoca Klebsiella pneumonia Enterobacter asburiae, Paenibacillus polymyxa, Pantoea rwandensis, Klebsiella variicola Pseudomonas spp.
Sebiawu et al.⁴⁹	2020	Ghana	15	12	Conventional culture method	1.0 ± 0.02 ×10¹ cfu/mL to 2.3 ±0.30×10⁶ cfu/mL	NA	Bacterial	Staphylococcus aureus Salmonella spp. Coliforms
Ayansina and Akinsola⁵⁰	2020	Nigeria	21	21	Conventional culture and molecular techniques	NA	NA	Bacterial Fungal	Providencia spp. Pantoea spp. Citrobacter spp. Serratia spp. Proteus spp. Klebsiella spp. Kluyvera spp. Enterobacter spp. Brenneria spp. Escherichia coli Edwardsiella spp. Salmonella spp. Cedecea spp. Pseudomonas spp. Yersinia spp. Aspergillus niger Mucor spp. Rhizopus stolonifera Candida stolonifera Aspergillus nidulans
Ngemenya et al.⁵¹	2019	Cameroon	8	8	Conventional culture method	NA	NA	Bacterial	Citrobacter freundii Citrobacter youngae Citrobacter spp. Enterobacter cloacae Escherichia coli Proteus mirabilis Proteus vulgaris Providencia rettgeri Salmonella typhi Salmonella spp.
Odo et al.⁵²	2023	Nigeria	8	8	Conventional culture method	1.8 × 10³ cfu/mL to 9.3 × 10³ cfu/mL	1.3 × 10³ cfu/mL to 2.5 × 10³ cfu/mL	Bacterial Fungal	Bacillus spp. Escherichia coli Staphylococcus aureus Enterobacter spp. Aspergillus niger Penicillium spp. Scedosporium spp. Phialophora parasiticum
Idu et al.⁵³	2010	Nigeria	17	17	Conventional culture method	1.3 × 10⁵ cfu/g to 6.7 × 10⁶ cfu/g	0 to 7.1 × 10⁶ cfu/g	Bacterial Fungal	Citrobacter spp. Klebsiella aerogenes Bacillus subtilis Diphtheroids Arizona spp. Staphylococcus epidermidis Serratia marcescens Pseudomonas aeruginosa Escherichia coli Proteus spp. Acinetobacter spp. Staphylococcus aureus Streptococcus spp. Aspergillus fumigatus Absidia spp. Mucor spp. Penicillium spp. Aspergillus niger Aspergillus ochraceus Saccharomyces cerevisiae Rhizopus nigricans
Omoruyi et al.⁵⁴	2023	Nigeria	50	20	Conventional culture method	2.8 × 10⁴ cfu/mL to 12.6 × 10⁸ cfu/mL	NA	Bacterial	Staphylococcus aureus Escherichia coli Klebsiella pneumoniae Klebsiella oxytoca Proteus mirabilis Enterobacter spp. Citrobacter spp.
Bello et al.⁵⁵	2019	Nigeria	10	8	Conventional culture method	2.5 × 10² cfu/mL to 4.4×10⁶ cfu/mL	NA	Bacterial	Bacillus subtilis Klebsiella pneumoniae Klebsiella oxytoca Staphylococcus aureus Enterobacter cloacae Enterobacter gergoviae Serratia marcescens
Ngari et al.⁵⁶	2013	Kenya	22	3	Conventional culture method	3.0 × 10³ cfu/mL to 2.6 × 10⁶ cfu/mL	NA	Bacterial Fungal	Escherichia coli Pseudomonas aeruginosa Salmonella typhi Candida albicans
Adounkpe et al.⁵⁷	2017	Benin	13	13	Conventional culture method	9.15±2.32 ×10⁷ cfu/mL to 3.65 ±0.87×10⁹ cfu/mL	1.6 ± 0.5 ×10⁵cfu/mL to 3.5 ±1.1×10⁶ cfu/mL	Bacterial Fungal	Total coliforms Escherichia coli Staphylococcus aureus Salmonella typhi Aspergillus flavus Aspergillus niger Penicillium expansum Fusarium solani
Bernadin et al.⁵⁸	2018	Cote d’Ivoire	188	188	Conventional culture method	1.0 ×10³ cfu/g to 4 ×10⁸ cfu/g	2.0 × 10⁴ cfu/g to 4.4 ×10⁷ cfu/g	Bacterial Fungal	Aerobic mesophilic bacteria Thermotolerant coliforms Escherichia coli Staphylococcus aureus Enterococci spp. Pseudomonas spp. Yeasts and moulds
Osei-Asare et al.⁵⁹	2023	Ghana	15	10	Conventional culture method	Less than 1.0 × 10 to TNC	Less than 1.0 × 10 to TNC	Bacterial Fungal	Escherichia coli Staphylococcus aureus Salmonella typhi Fungi
Usanga et al.⁶⁹	2023	Nigeria	50	50	Conventional culture method	NA	NA	Fungal	Aspergillus niger Aspergillus flavus
Bashir et al.⁶⁰	2017	Nigeria	12	12	Conventional culture method	3.1 × 10⁵ cfu/mL to 1.85 × 10⁶ cfu/mL	3.1 × 10⁵ cfu/mL to 1.85 × 10⁶ cfu/mL	Bacterial Fungal	Staphylococcus aureus Bacillus spp. Escherichia coli Salmonella typhi Aspergillus spp. Penicillium spp.
Onyambu et al.⁶¹	2013	Kenya	30	30	Conventional culture method	6.0 × 10⁵ cfu/mL to 1.50 × 10¹⁰ cfu/mL	5.0 × 10⁵ cfu/mL to 1.56 × 10⁹ cfu/mL	Bacterial Fungal	Klebsiella pneumoniae Klebsiella oxytoca Enterobacter cloacae Bacillus flexus Bacillus safensis Bacillus subtilis Bacillus pumilus Staphylococcus aureus Escherichia coli Salmonella spp. Enterobacter aerogenes Chryseomonas luteola Shigella spp. Flavobacterium spp. Enterobacter agglomerurans Serratia marcescens Kocuria rosea Rhizobium spp. Pseudomonas aeruginosa Aspergillus spp. Fusarium spp. Candida spp. Penicillium spp. Torula spp. Rhizopus spp.
Kira et al.⁶²	2021	Tanzania	50	44	Conventional culture method	9.09×10⁴ to 1.64 ×10⁸ cfu/g per mL	NA	Bacterial	Staphylococcus aureus Escherichia coli Enterobacter spp. Bacillus spp. Staphylococcus epidermidis Klebsiella pneumoniae Pseudomonas aeruginosa
Dabo et al.⁶³	2024	Nigeria	30	30	Conventional culture method	NA	NA	Bacterial Fungal	Salmonella spp. Escherichia coli Klebsiella spp. Proteus spp. Staphylococcus spp. Aspergillus flavus Aspergillus niger Aspergillus ochraceus Rhizopus stolonifera Trichosporon mucoides
Omoruyi et al.⁶⁴	2024	Nigeria	50	20	Conventional culture method	NA	NA	Bacterial	Staphylococcus aureus Escherichia coli Klebsiella pneumoniae Klebsiella oxytoca Proteus mirabilis Enterobacter spp. Citrobacter spp.
Osei et al.⁶⁵	2024	Ghana	3	3	Conventional culture method	3.6 ± 0.03 × 10³ cfu/mL to 4.1 ± 0.19 ×10³ cfu/mL	1.2 ± 0.19 ×10³ ± 0.19 cfu/mL to 1.6 ± 0.30 cfu/mL×10³ ± 0.30 cfu/mL	Bacterial Fungal	Aerobic bacteria Yeast and mould
Onyemelukwe et al.⁶⁶	2019	Nigeria	80	80	Conventional culture method	2.1 × 10³ cfu/mL to 9.0 × 10⁶ cfu/mL	1.1 × 10³ cfu/mL to 8.0 × 10⁵ cfu/mL	Bacterial Fungal Parasitic	Bacillus spp. Pseudomonas aeruginosa Escherichia coli Enterobacter spp. Staphylococcus aureus Klebsiella spp. Salmonella spp. Aspergillus flavus Rhizopus spp. Geotrichum candidum Aspergillus niger Trichophyton rentagrophytes Microsporium canis Penicillium spp. Mucor spp. Syncephilastrum racemosus Ascaris lumbricoides Hookworm Toxocora canis Entamoeba coli Giardia infestinalis Entamoeba histolytica/dispar
Addotey and Nyansah⁶⁷	2016	Ghana	11	11	Conventional culture methods	NA	1.1 × 10² cfu/mL to 1.6 × 10⁴ cfu/ml	Bacterial Fungal	Staphylococcus aureus Moulds and yeasts
Udeogu et al.⁶⁸	2020	Nigeria	44	27	Conventional culture methods	7.0 × 10⁵ cfu/mL to 8.9 × 10⁶ cfu/mL	NA	Bacterial	Klebsiella pneumoniae Enterococcus faecalis Staphylococcus aureus Escherichia coli Proteus spp. Salmonella spp.

Figure 2.

Geographical distribution of the included articles.

Of the 50 studies reviewed, 49 (98%) reported on bacterial contaminants, 35 (70%) reported on fungal contaminants, and only 1 (2%) study reported on parasitic contaminants in herbal medicines. Some studies examined multiple types of contaminants, resulting in a combined total that exceeds the total number of individual studies. Conventional culture and identification methods, encompassing gram staining, biochemical reactions, and physiological techniques, were employed in 96% of the studies to identify bacterial, fungal, and parasitic contaminants in herbal medicines. Molecular techniques for isolation and identification were used in only 4% of the studies. The prevalence of microbial contamination in herbal medicines varied widely, ranging from 14% to 100%.

Collectively, the included studies examined 1996 herbal medicine samples, with 1791 of the samples harbouring microbial contamination. This equates to an overall contamination prevalence of 90% in herbal medicines across Africa. Sixty-two percent (62%) of the reviewed studies reported a 100% prevalence of microbial contamination. The majority of studies included in this review, 39 (78%), were published from 2014 to 2024, while 11 (22%) were published between 2000 and 2013.

Bacterial contaminants of herbal preparations in Africa

A significant number of studies (98%) reported diverse bacterial contaminants in herbal medicines.^{8,10,22
–68} Across these studies, 70 bacteria from 37 different genera were isolated. Escherichia coli emerged as the most frequently identified bacteria, reported in 62% of the studies. Other commonly reported bacterial contaminants include Staphylococcus aureus (60%), Bacillus spp. (54%), Pseudomonas spp. (46%), Salmonella spp. (44%), Klebsiella spp. (44%), Enterobacter spp. (38%), Proteus spp. (22%), Serratia spp. (16%), Citrobacter spp. (16%), Enterococcus spp. (12%), Streptococcus spp. (10%), Pantoea spp. (10%), Shigella spp. (8%), Acinetobacter spp. (8%), Providencia spp. (6%), Rahnella spp. (4%), Chryseomonas spp. (4%), and Moraxella spp. (4%). Each of the following bacterial contaminants was reported in 2% of the included studies: Edwardsiella spp., Cedecea spp., Flavimonas spp., Stenotrophomonas spp., Ewingella spp., Bordetella spp., Pasteurella spp., Aeromonas spp., Arizona spp., Kocuria spp., Rhizobium spp., Leclecia spp., Sphingomonas spp., Raoultella spp., Paenibacillus spp., Corynebacterium spp., Micrococcus spp., and Yersinia spp. Figure 3 illustrates the percentage distribution of the common bacterial isolates identified in this review.

Figure 3.

Percentage frequency of bacterial isolates identified in the included studies.

From the studies included in this review, reports on the bacterial loads of the various herbal medicines analysed, revealed varying levels of contamination across different countries. The bacterial loads documented in this review generally ranged from 0 cfu/mL to 3.54 × 10¹² cfu/mL. The highest bacterial load recorded (3.54 × 10¹² cfu/mL) was reported in Nigeria by Igbeneghu and Lamikanra.³⁶ The samples in this study were sourced from unregulated herbal medicines on the market. Similarly, another study by Nwankwo and Olime,²⁸ which investigated microbial contamination in registered herbal preparations on the Nigerian market, reported bacterial loads ranging from 3.10 × 10² cfu/mL to 2.56 × 10³ cfu/mL in liquid formulations, and 9.0 × 10¹ cfu/g to 1.5 cfu/g × 10² cfu/g in powdered herbal preparations.

In a study conducted in Nigeria by Tatfeng et al.,³³ it was noted that ‘schnapps’ and palm wine–based preparations were mostly contaminated with Bacillus spp. (aerobic spore bearers), while water-based preparations had several bacterial isolates, including Staphylococcus spp., Pseudomonas aeruginosa, Escherichia coli 0157, Proteus mirabilis, Enterococcus faecalis, Serratia marcescens, Staphylococcus aureus, and Bacillus spp.

Also in the studies outlined, Brooks and Takim²⁵ reported a Total Viable Bacterial Count (TVBC) of 2.2 × 10⁴ cfu/g to 5.6 × 10⁴ cfu/g for solid dosage forms and 3.8 × 10⁴ cfu/mL to 6.8 × 10⁴ cfu/mL for liquid forms of herbal medicines sold in Calabar, Nigeria. Nwankwo and Olime²⁸ reported a Total Heterotrophic Bacterial Count (THBC) of 3.1 × 10² cfu/mL to 2.65 × 10³ cfu/mL for liquid preparations and 1.1 × 10² cfu/g to 1.5 × 10 ²cfu/g for powdered preparations. Walusansa et al³¹ in a study conducted in Uganda reported a mean viable load of 126.407 × 10⁴ cfu/mL or g across 140 samples. Kaume et al.³⁵ reported bacterial loads ranging from 3.03 × 10⁴ cfu/mL to 4.22 × 10⁵ cfu/mL in some herbal medicines in Kenya.

Omoruyi et al.⁵⁴ in Nigeria found microbial counts ranging from 2.8 × 10⁴ cfu/mL to 3.1 × 10⁴ cfu/mL for regulated products and 3.8 × 10⁴ cfu/mL to 12.6 × 10³ cfu/mL for unregulated products. A study conducted by Onyambu et al.⁶¹ on regulated and unregulated herbal medicines in Kenya reported a bacterial load count of 1.50 × 10¹⁰ cfu/mL in unregulated herbal medicines and counts below 100 cfu/mL in registered herbal products. Adounkpe et al.⁵⁷ reported bacterial loads ranging from 9.15 × 10⁷ cfu/mL to 3.65 × 10⁹ cfu/mL in herbal medicines from Benin. Osei-Adjei et al.⁴⁵ reported bacterial loads ranging from 1.0 × 10² cfu/mL to 1.0 × 10⁹ cfu/mL in herbal medicines from Ghana. Kira et al.⁶² reported a mean bacterial load of 1.64 × 10⁸ cfu/mL in herbal medicines from Tanzania.

Fungal contaminants of herbal medicines in Africa

Fungal contaminants were reported in 35 (70%) studies.^{10,24-29,32,33,35-43,45-47,50,52,53,56-61,63,65-67,69} Forty (40) fungal species from 24 different genera were identified (Table 1). Aspergillus spp. was the most commonly reported fungal species, appearing in 40% of the studies. This was followed by Penicillium spp. (28%), Candida spp. (24%), Mucor spp. (20%), Rhizopus spp. (20%), Fusarium spp. (8%), Cladosporium spp. (6%), Saccharomyces spp. (6%), Trichosporon spp. (4%), Scedosporium spp. (4%), and Geotrichum spp. (4%). Other fungal contaminants reported include Phaeoacremonium spp., Curvularia spp., Cryptococcus spp., Trichoderma spp., Alternaria spp., Mycelia spp., Rhodotorula spp., Sporobolomyces spp., Phialophora spp., Torula spp., Trichophyton spp., Microsporium spp., and Syncephilastrum spp., each reported in 2% of the reviewed studies.

Several studies included in this review also documented a wide range of fungal loads in herbal medicines. The total fungal loads reported across the studies ranged from 0 cfu/mL to 3.54 × 10¹² cfu/mL. Some of the highest fungal loads reported in this review were: 3.54 × 10¹² cfu/mL recorded in Nigeria,³⁶ 1.60 × 10⁹ cfu/mL from Sierra Leone,³⁷ 6.0 × 10⁸ cfu/mL from Lesotho,²⁷ 1.3 × 10⁸ cfu/mL from Nigeria,⁴³ 4.4 × 10⁷ cfu/g recorded in Cote d’Ivoire,⁵⁸ 4.7 × 10⁷ cfu/mL³³ and 1.5 × 10⁷ cfu/mL both recorded in Nigeria. Akande et al.⁴⁷ reported total fungal counts of 1.0 × 10⁵ cfu/mL to 8.0 × 10⁵ cfu/mL in herbal medicines from Nigeria. The fungal counts as presented by the studies included are shown in Table 1. Figure 4 shows the percentage frequency of the most reported fungal isolates.

Figure 4.

Percentage frequency of fungal isolates identified in the included studies.

Parasitic contaminants of herbal medicines in Africa

Only 1 study (2%) reported parasite contamination in herbal medicines in the reviewed studies. The study by Onyemelukwe et al.⁶⁶ reported a 53% occurrence of parasites in 80 herbal medicine samples from Nigeria. Ascaris lumbricoides, was the most prevalent parasite in that study, detected in 53.7% of the samples, followed by hookworm ova (19.5%), and Toxocara canis (12.2%). The least prevalent parasites were Entamoeba coli, Giardia infestinalis, and Entamoeba histolytica/dispar each found in 4.9% of the samples.

Discussion

The increasing use of herbal medicines and other crude concoctions in Africa raises concerns about their safety to consumers, particularly relating to their microbial quality. This study analysed fifty studies that investigated the prevalence and loads of microbial contaminants in herbal medicines across Africa; Nigeria, Ghana, Kenya, South Africa, Tanzania, Cote d’Ivoire, Malawi, Cameroon, Sierra Leone, Benin, Lesotho, and Uganda. Most (78%) of these studies were conducted in the recent decade (2014-2024). This trend is supported by other findings,¹² indicating a significant increase in research addressing the microbial contamination of herbal medicines in Africa.

This review reported on bacterial, fungal, and parasitic contaminants in herbal medicines across the African region. The majority of included studies (98%) reported on bacterial contaminants. Escherichia coli was the most reported bacterial pathogen in herbal medicines across the African region. This finding is consistent with the report from the study conducted by Walusansa et al, which identified Escherichia coli as the most prevalent bacterial contaminant in herbal medicines.¹² Findings from another study conducted by Opuni et al.,¹⁵ also reported Escherichia coli as the most reported bacterial contaminant found in herbal medicines across low–and middle– income countries. The presence of this pathogen in herbal medicines suggests possible faecal contamination, raising concerns about the potential for direct or indirect exposure to human or animal waste during preparation.^27,31 According to the World Health Organisation, (WHO),⁷⁰ the presence of E. coli not only indicates faecal contamination but also raises concerns about the potential presence of more virulent strains, such as shiga toxin-producing E. coli. These strains are implicated in life–threatening diseases such as haemolytic uraemic syndrome, particularly in vulnerable populations like young children, the elderly, and HIV/AIDS patients.^15,70 Notably, some studies included in this review^26,35 investigated herbal medicines marketed to HIV/AIDS patients. These studies revealed alarming levels of bacterial contamination exceeding acceptable limits. As reported in these studies, liquid formulations recorded bacterial counts as high as 1.19 × 10⁹ cfu/mL,²⁶ while solid dosage forms recorded 7.1 × 10⁸ cfu/g,³⁵ exceeding the acceptable limits of 10⁵ cfu/mL for liquid samples and 10⁷ cfu/mL for solid samples.⁷¹ This poses a significant health threat to an already immunocompromised population.

This review also identified Staphylococcus aureus, Bacillus spp., Pseudomonas spp., and Salmonella spp. as commonly reported bacterial pathogens (60%, 54%, 46%, and 44% of included studies respectively) from herbal medicines in Africa. These findings are consistent with findings from low–and middle–income countries in other regions. Studies conducted by Opuni et al.¹⁵ and De Souza Lima et al.¹¹ identified Salmonella spp., Bacillus spp., Pseudomonas aeruginosa and Staphylococcus spp. as common bacterial pathogens in herbal medicines. These organisms which are also indications of faecal contamination, reveal poor hygiene conditions in the preparation and storage of these herbal medicines, thus making them unsafe for consumption.^15,72 In this review, Govender et al.²⁶ identified diarrhoeal toxins produced by Bacillus cereus in herbal medicines from South Africa. Additionally, other studies^26,73,74 highlight the potential health risks posed by toxins when consumed. The potential for severe infectious diseases among the African population due to contaminated herbal remedies is a serious concern, given the presence of numerous medically important pathogens. Staphylococcus aureus, for example, which was reported in 60% of studies included in this review causes staphylococcal gastroenteritis, scalded–skin syndrome, toxic shock syndrome, endocarditis, lung infection, folliculitis, among other diseases.^75
-77 These diseases are life–threatening in older people and immunocompromised adults.⁷⁶

According to the World Health Organisation (WHO), ‘Salmonella and Shigella species must not be present in herbal medicines intended for internal use, at any stage’.⁷¹ Contrary to this guideline, Salmonella spp., and Shigella spp. were reported in 44% and 8% of the studies respectively. These organisms have the potential to cause large disease outbreaks due to their low infectious dose.⁷⁸ They are responsible for a significant disease burden worldwide, causing diarrhoea and a spectrum of associated symptoms, from mild to life–threatening.⁷⁹ The CDC estimates that Salmonella spp. causes approximately 1.4 million infections, 26, 500 hospitalisations, and over 400 deaths annually in the United States.⁸⁰ This poses a significant threat to public health in Africa, where many people rely on herbal remedies and may lack access to adequate medical care. Similar to our findings in Africa, gram–negative bacteria such as Escherichia coli, Klebsiella spp., Pseudomonas spp., Shigella spp., and Salmonella spp. in addition to several species of Staphylococcus have been reported as major contaminants in herbal medicines from other continents, particularly Asia.^81
-83

Another popular finding across multiple studies included in this review is the presence of fungal isolates from the genera Aspergillus, Penicillium, Candida, Mucor, Rhizopus, Fusarium, Cladosporium, and Scedosporium in herbal medicines across the African region. These fungal species have been identified in herbal medicines across various regions globally as evidenced in studies conducted by De Souza et al., Kneifel et al., Lee & Yoon, Opuni et al., and Zheng et al.^15,72,84
-86 The study by Kneifel et al.⁸⁴ revealed that fungal isolates in herbal medicines can degrade active ingredients reducing their effectiveness, and potentially produce mycotoxins. These toxins are mainly produced by fungi from the genera Aspergillus, Penicillium and Fusarium.⁸⁷ Exposure to these toxins can have devastating effects on human health, potentially leading to liver cancers, weakened immunity, altered protein metabolism, seizures, and respiratory problems among other health complications.^88
-90

Herbal medicines to a large extent are mostly contaminated with bacterial and fungal elements.¹⁵ However, one study included in this review reported the contamination of herbal products from Nigeria with parasite forms such as helminths and protozoans. The study by Onyemelukwe et al.,⁶⁶ reported the presence of helminth eggs and protozoan cysts in herbal preparations at a staggering 53% occurrence. The parasites found in these herbal preparations included Ascaris lumbricoides, hookworm, Toxocara canis, Entamoeba coli, Entamoeba histolytica/dispar and Giardia intestinalis.⁶⁶ Data from other regions such as Asia supports the occurrence of parasitic contaminants in herbal medicines. A study conducted by Posadzki et al.,²¹ found parasitic contaminants similar to those identified in the study from Nigeria in herbal medicines.

The problem of microbial contamination of herbal products in Africa is exacerbated by widespread environmental pollution and unsanitary conditions^66,91 which is common in Africa. Several studies included in this review^{8,10,22,24-27,34,44,56} attributed the high prevalence of microbial contamination in herbal medicines to a combination of factors, including lack of regulation, and pollution throughout the production chain, from harvesting raw materials, to handling, processing, storage, and transportation. According to Onyemelukwe et al., the trees and plants from which medicinal preparations are made could have microorganisms adhered to their stems, barks, leaves, flowers, fruits, and roots eventually leading to contamination of the product.⁶⁶ Other factors contributing to the high prevalence of microbial contamination in herbal medicines as reported in the reviewed studies include the use of untreated water supply, poor quality of packaging materials, use of contaminated containers, working from polluted faecal environments, and poor personal hygiene behaviours during handling.^29,31-33,59

A survey conducted by the World Health Organisation (WHO) in 2019, indicated that 43% of African member states regulate herbal medicines, compared to 26% in 2005.⁴ However, despite the progress in regulatory efforts, this study found a significant 90% overall prevalence of microbial contamination in herbal medicines, highlighting the need for stricter regulations in the African region. The prevalence of microbial contamination in herbal medicines is a public health concern in Africa. To address this challenge, it is important that existing regulations are enforced and novel regulations adopted in countries where they are lacking. Also, producers of herbal medicines should ensure strict quality control measures and Good Manufacturing Practices (GMP) are followed throughout the production and distribution processes to minimise the proliferation of microorganisms in these products. Failure to address this issue could lead to widespread health problems in Africa. Research on the microbiological safety of herbal medicines in Africa must expand beyond fungal and bacterial contaminants to include parasites for a comprehensive understanding of the unique challenges associated with these remedies.

Limitations of the Study

While this systematic review provides valuable insights, it is subject to some key limitations. Firstly, the literature search was restricted to peer-reviewed studies published in English language, potentially excluding grey literature and other relevant studies not published in English. Secondly, the studies captured in this review were mainly from the western, eastern, and southern parts of Africa, limiting its generalisability.

Conclusion

This systematic review provided a comprehensive overview of the microbial contaminants reported in herbal medicines across Africa, revealing a disturbingly wide range of bacterial, fungal, and parasitic species with varying degrees of contamination. The presence of pathogens such as Escherichia coli, Staphylococcus aureus, Bacillus spp., Pseudomonas spp., Salmonella spp., Klebsiella spp., Shigella spp., Aspergillus spp., Penicillium spp., Candida spp., Mucor spp. and Entamoeba histolytica among others, poses a significant risk to consumer safety. The findings of this review underscore the urgent need for stricter regulations and quality control measures to ensure the safety of herbal medicine products in Africa, ultimately protecting the health and well-being of consumers.

Supplemental Material

sj-docx-1-ehi-10.1177_11786302241293345 – Supplemental material for Microbial Contamination of Herbal Medicines in Africa, 2000-2024: A Systematic Review

Supplemental material, sj-docx-1-ehi-10.1177_11786302241293345 for Microbial Contamination of Herbal Medicines in Africa, 2000-2024: A Systematic Review by Wisdom K Ahiabor, Samuel Darkwah and Eric S Donkor in Environmental Health Insights

Supplemental Material

sj-docx-2-ehi-10.1177_11786302241293345 – Supplemental material for Microbial Contamination of Herbal Medicines in Africa, 2000-2024: A Systematic Review

Supplemental material, sj-docx-2-ehi-10.1177_11786302241293345 for Microbial Contamination of Herbal Medicines in Africa, 2000-2024: A Systematic Review by Wisdom K Ahiabor, Samuel Darkwah and Eric S Donkor in Environmental Health Insights

Footnotes

Funding:

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was funded by the National Institutes of Health, USA, through the “Application of Data Science to Build Research Capacity in Zoonoses and Food-Borne Infections in West Africa (DS-ZOOFOOD) Training Programme” hosted at the Department of Medical Microbiology, University of Ghana Medical School (Grant Number: UE5TW012566-01). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Declaration of conflicting interests:

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Author Contributions

Conceptualisation, ESD; methodology, WKA, SD, and ESD; validation, SD, and ESD; formal analysis, WKA, and SD; resources, ESD; data curation, WKA; writing—original draft preparation, WKA, SD and ESD; writing—review and editing, WKA, SD, and ESD; visualisation, WKA, and SD; supervision, ESD.

ORCID iDs

Wisdom K Ahiabor

Samuel Darkwah

Eric S Donkor

Supplemental Material

Supplemental material for this article is available online.

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