Remous Ocloo1*
Justin Nyasinga2,3,4
Zubair Munshi2
Aisha Hamdy5
Tessa Marciniak6
Manonmani Soundararajan6
Mae Newton-Foot1,7
Wilma Ziebuhr6
Adebayo Shittu8
Gunturu Revathi2
Alaa Abouelfetouh5,9
Andrew Whitelaw1,7- 1Division of Medical Microbiology and Immunology, Stellenbosch University, Stellenbosch, South Africa
- 2Department of Pathology, Aga Khan University Hospital, Nairobi, Kenya
- 3Institute of Science, Technology and Innovation, Pan African University, Nairobi, Kenya
- 4Department of Biomedical Sciences and Technology, The Technical University of Kenya, Nairobi, Kenya
- 5Department of Microbiology and Immunology, Faculty of Pharmacy, Alexandria University, Alexandria, Egypt
- 6Institute for Molecular Infection Biology, University of Wuerzburg, Wuerzburg, Germany
- 7National Health Laboratory Service, Tygerberg Hospital, Cape Town, South Africa
- 8Department of Microbiology, Obafemi Awolowo University, Ile-Ife, Nigeria
- 9Department of Microbiology and Immunology, Faculty of Pharmacy, Alamein International University, Alamein, Egypt
Introduction: Staphylococci other than Staphylococcus aureus (SOSA) in animals are becoming more pathogenic and antibiotic resistant and can potentially disseminate to humans. However, there is little synthesized information regarding SOSA from animals in Africa. This systematic review provides a comprehensive overview of the epidemiology and antimicrobial resistance of SOSA in companion animals (pets) and livestock in Africa.
Method: This systematic review (PROSPERO-CRD42021252303) was conducted according to the PRISMA guidelines, and 75 eligible studies from 13 countries were identified until August 2022. Three electronic databases (Pubmed, Scopus and Web of Science) were employed.
Results: The frequently isolated SOSA were S. epidermidis, S. intermedius, S. pseudintermedius, S. xylosus, S. chromogenes, S. hyicus, M. sciuri, S. hominis, and S. haemolyticus. Thirty (40%) studies performed antibiotic susceptibility testing (AST). Penicillin (58%) and tetracycline (28%) resistance were most common across all SOSA with high rates of resistance to aminoglycosides, fluoroquinolones, and macrolides in some species. Resistance to last-resort antibiotics such as linezolid and fusidic acid were also reported. Limited data on strain typing and molecular resistance mechanisms precluded analysis of the clonal diversity of SOSA on the continent.
Conclusion: The findings of this review indicate that research on livestock-associated SOSA in Africa is lacking in some regions such as Central and Western Africa, furthermore, research on companion animals and more advanced methods for identification and strain typing of SOSA need to be encouraged.
Systematic review registration: https://www.crd.york.ac.uk/prospero/, identifier: CRD42021252303.
Introduction
Staphylococci colonize the skin and mucous membranes of a wide range of vertebrate hosts and account for several human and animal diseases (1–4). Staphylococci other than Staphylococcus aureus (SOSA) is a relatively new term, encompassing largely coagulase-negative staphylococci, including two coagulase-positive staphylococcal species (S. pseudintermedius and S. schleiferi) (2). There are increasing reports of SOSA infections associated with implantable foreign bodies and sepsis, particularly among newborns and preterm neonates (5). Moreover, some SOSA (e.g., S. pseudintermedius, S. schleiferi, and S. felis) are important pathogens in veterinary medicine (6). SOSA infections are a global economic problem in the animal production sector (7–11). SOSA are largely responsible for mastitis in milk-producing animals, leading to reduced milk production (12).
Antimicrobials are administered to animals to enhance growth and prevent infection. However, the doses of antimicrobials dispensed by practitioners in animal husbandry are mostly sub-therapeutic and contribute to the emergence of antimicrobial resistance (AMR) (13–15). The spread of AMR genes may be exacerbated by trading with animals between farms and other animal husbandry practices (16, 17).
High resistance rates have been described in SOSA from animals. Tetracycline resistance has been described in SOSA isolates from normal and subclinical mastitic buffalo milk in Egypt: 100% in S. lugdunensis and S. hominis, and 66.6% in S. epidermidis (18). SOSA isolates recovered from turkey farms in Egypt were also resistant to tetracycline (100%), oxacillin (92.3%) and daptomycin (89.7%) (19). In Turkey, 75% of SOSA recovered from raw milk were resistant to erythromycin (20) and in South Africa, 51% of SOSA isolates from subclinical mastitis cow milk samples were multidrug resistant (MDR) (21). Antimicrobial-resistant SOSA (AMRSOSA) in livestock and companion animals pose an economic threat to the livestock industry and a risk for spill-over into the human environment, threatening public health (22–24).
SOSA are considered less pathogenic than S. aureus and this perception has led to limited knowledge on the virulence, prevalence, and dissemination of SOSA, particularly in animals (25, 26). However, in recent years, resistance to last-resort antibiotics has been described in SOSA (19, 27, 28). There is also evidence that SOSA and S. aureus exchange virulence and resistance genes continuously in the natural environment, which is a potential risk to the empiric treatment of S. aureus infections (29–33). For example, Mammaliicoccus sciuri, formerly known as Staphylococcus sciuri, is postulated to be the origin of mecA and the precursor to the evolution of the staphylococcal cassette chromosome mec (SCCmec) element (34, 35). The methicillin resistance gene (mecA) encodes an alternative penicillin-binding protein (PBP2A) (36, 37), which confers resistance to the β-lactam class of antibiotics such as penicillins and cephalosporins.
Systematic reviews on S. aureus in animals have observed that both animal clonal complex (CC) 398, CC130, CC133 and human-associated lineages (CC1, CC15, CC72, CC80, CC10, and CC152) are common in Africa. Methicillin resistant S. aureus (MRSA) prevalence ranges from 0 to 3 % (38, 39). However, the epidemiology of SOSA in companion animals and livestock in Africa is not well-described, despite the potential for transfer of staphylococci and their resistance mechanisms from these animals to humans. This study aims to provide a comprehensive overview of the published data describing the epidemiology and antimicrobial resistance of SOSA in companion animals and livestock in Africa.
Methods
This systematic review was registered on https://www.crd.york.ac.uk/prospero/ (PROSPERO-CRD42021252303) and conducted following the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines (40).
Literature search strategies
A literature search of relevant articles in PubMed, Scopus, and Web of Science, published from 1991 to 2022, was conducted and retrieved until August 2022 using the search terms described in Supplementary material 1. The results were transferred onto Microsoft Excel, and duplicates were removed. Titles and abstracts were screened, and full-text articles were assessed for eligibility. All searches and screenings were done by two independent reviewers each, and discrepancies were resolved by consensus.
Eligible article selection
Inclusion criteria
Eligible studies included reports on SOSA isolated from companion animals and livestock in Africa and published in peer-reviewed English journals. Other criteria for inclusion were descriptions of population size and laboratory methods. Mammaliicoccus sciuri was included in this study as it was previously regarded as S. sciuri.
Exclusion criteria
Studies not published in English journals, published in predatory journals (according to Beall's list, 2021), which did not report on primary data, and those which reported on S. aureus only or did not perform speciation of SOSA were excluded. Review articles, notes, e-mails, editorials, articles without original data and studies that only described animal products and wild animals were also excluded.
Data extraction and synthesis
The following data were extracted onto Microsoft Excel: first author, year of publication, study design, country/region, type of animals, number of animals, type of samples, number of samples, and year of sample collection. Other information included species isolated, number of isolates, susceptibility data for various classes of antibiotics (fluoroquinolones, cephalosporins, penicillins, aminoglycosides, macrolides, and polymyxins), resistance genes, laboratory methods, and strain types. Data extraction was performed by two independent reviewers and discrepancies were resolved by consensus. The data were stratified using the United Nations geoscheme subregion classification (https://unstats.un.org/unsd/methodology/m49/).
Data interpretation
Antibiotic resistance rates were only reported for a species when a minimum of 30 isolates were tested (41). Antibiotic resistance rates for each species were calculated using the number of resistant isolates (NR) and total number of isolates tested (NT).
Differences between antibiotic rates in carriage and pathogenic SOSA were calculated using Fisher exact and Chi squared tests where appropriate.
Results
Study description
The systematic search of the three databases yielded 9,160 articles. After de-duplication and exclusion by title and abstract screening, 395 full-text articles were screened, of which 75 were considered eligible based on our inclusion criteria (Figure 1). The majority of the studies (97%; n = 73), were published between 2000 and 2022, with 69% of the studies (n = 52) published between 2012 and 2022. According to regions, Northern Africa (n = 28) had the highest number of eligible studies, followed by Eastern Africa (n = 26), Western Africa (n = 11), and Southern Africa (n = 10) (Figure 2). No articles were available from Central Africa.
Figure 1. PRISMA flow diagram of the detailed search process and study selection.
Figure 2. Diversity of livestock and domestic animals in which SOSA was described in Africa. Adapted from the United Nations geoscheme subregions African Map. n, number of articles.
Of the 75 eligible studies, 62 described SOSA in livestock, 12 in companion animals, and one included both livestock and companion animal. Of the reports from livestock, 17 were performed on subsistence farms, nine on commercial farms, and the rest (n = 49) did not provide information on farm type. Overall, 46 reports were from diseased animals, 17 from healthy animals, and ten from diseased and healthy animals; while 2 did not provide information. Dogs were the most common companion animal investigated, in 12 studies, while cows and goats were the main livestock investigated, in 32 and 13 studies, respectively. Figure 2 represents the diversity of animals in which SOSA were described in Africa. Milk was the leading sample type screened, representing 65% (n = 49) of the eligible studies. Most SOSA were isolated from cows with mastitis (Table 1).
Table 1. Sources, clinical significance & geographical distribution of Staphylococci other than S. aureus (SOSA) in Africa.
Distribution of SOSA
The frequently isolated SOSA in Africa were S. epidermidis (23%; n = 784), S. intermedius (14%; n = 446), S. pseudintermedius (11%; n = 371), S. xylosus (10%; n = 346), S. chromogenes (9.0%; n = 303), S. hyicus (4.7%; n = 157), M. sciuri (4.5%; n = 151), S. hominis (3.9%; n = 130), and S. haemolyticus (3.7%; n = 123) (Figure 3). S. xylosus was most frequently reported in Northern Africa, S. intermedius/S. pseudintermedius in Southern Africa, while S. epidermidis was predominant in Eastern and Western Africa (Table 1). API-Staph and BD Phoenix were the common biochemical tests employed to identify SOSA, in 64% (n = 48) studies (Supplementary material 2).
Figure 3. Regional distribution of SOSA in Africa. SOSA isolates were classified as “Others” when the total number included in the review was <100. Isolates (n = 177) in which colonization and infection were not distinguished were excluded. Eastern Africa (Ethiopia, Kenya, Rwanda, Tanzania, Uganda & Zimbabwe), Northern Africa (Algeria, Egypt, Libya & Tunisia), Southern Africa (Botswana & South Africa), Western Africa (Nigeria).
Antibiotic susceptibility of SOSA
Thirty (40%) studies identified SOSA to the species level and performed antibiotic susceptibility testing (AST), of these only five (13%) were published prior to 2012. The Kirby Bauer disc diffusion method was widely utilized for AST (87%; n = 26) and the zone of inhibition was mostly interpreted using Clinical and Laboratory Standards Institute (CLSI) guidelines (81%; n = 21) (Supplementary material 2a).
Generally, data on methicillin resistance in SOSA was lacking. However, methicillin resistance rates were high among S. pseudintermedius (89%; n = 83) and M. sciuri (54%; n = 37), S. xylosus (45%; n = 37), and S. epidermidis (44%; n = 14) isolates. The typical human-associated SOSA showed high rates of penicillin resistance, S. epidermidis (64%), S. haemolyticus (63%), and S. hominis (96%), however, there was less resistance to glycopeptides and rifampicin. High rates of fluoroquinolone resistance were also observed in S. epidermidis (69%), S. hyicus (56%), S. xylosus (42%), and M. sciuri (36%). Aminoglycoside resistance was high in S. xylosus (31%), M. sciuri (36%), and S. hominis (33%) compared to the other SOSA. Lincosamide resistance was also high in M. sciuri (54%) and S. xylosus (31%) and M. sciuri demonstrated high rates of macrolide resistance (56%; n = 32). Overall, in SOSA, resistance to penicillin (58%) and tetracycline (28%) were most common (Supplementary material 2b). A few studies (n = 5) reported on susceptibility to last-resort antibiotics. Linezolid resistance was described in S. intermedius (n = 5), S. xylosus (n = 3), S. equorum (n = 1) and S. epidermidis (n =1) and resistance to fusidic acid was observed in S. pseudintermedius (n = 4), M. sciuri (n = 5), S. xylosus (n = 3), and S. hominis (n = 1) (Supplementary material 3). Figure 4 shows the rate of antibiotic resistance in SOSA species commonly encountered in the clinical setting. However, we were unable to stratify data geographically due to insufficient data from other regions.
Figure 4. Rate of antibiotic resistance of clinically significant SOSA. AMI, Aminoglycoside; MAC, Macrolide; PEN, Penicillin; TET, Tetracycline; MET, Methicillin. “n” Denotes the number of isolates tested against a particular antibiotic. “NA” denotes not applicable.
Higher rates of aminoglycoside, fluoroquinolone, lincosamide, macrolide, rifampicin and methicillin resistance have been seen in carriage SOSA compared to pathogenic SOSA (Supplementary material 4).
Antibiotic resistance mechanisms and strain typing
Fifteen (20%) studies performed molecular screening for AMR genes and reported the presence of the mecA gene in at least one member of the SOSA. The mecA was detected in S. pseudintermedius (n = 49), S. sciuri (n = 31), S. intermedius (n = 27), S. xylosus (n = 23), S. epidermidis (n = 12), S. schleiferi (n = 10), S. haemolyticus (n = 8), S. hominis (n = 3), S. hyicus (n = 2), and S. chromogenes (n = 1) (Supplementary material 5). Only three studies reported on SCCmec typing: SCCmec type V was noted in S. warneri, and SCCmec types I and IVa were detected in S. epidermidis. Only one study reported on sequence types (STs), diverse STs were described in S. delphini and S. pseudintermedius (Supplementary material 6).
Discussion
Diverse SOSA were recovered from clinical and non-clinical samples from livestock and companion animals in Africa. The most common species include S. epidermidis, S. pseudintermedius, S. xylosus, and S. chromogenes. S. pseudintermedius was most commonly isolated in pets and S. epidermidis in livestock. However, there is lack of data on certain species in some countries such Botswana, Nigeria and Libya. We recommend that studies focus more on the following SOSA organisms which can also help understand the burden of SOSA infections in animals in Africa: S. intermedius, S. xylosus and S. chromogenes. S. pseudintermedius is considered as typical zoonotic commensal organism in the ears and skin of dogs and birds (79, 91). It is responsible for skin and soft tissue infections in dogs (67, 100), however in humans it is predominantly associated with infected dog bites and bacteraemia (113, 114). Surprisingly, none of the dogs from Western Africa (Nigeria) harbored S. pseudintermedius (104, 105, 108). S. xylosus is ubiquitous bacterium which is naturally occurring in the soil, food and on surfaces (115–117). Some strains are associated with opportunistic infections in humans (118, 119). There were no livestock associated infections/colonisations due to S. xylosus reported in Botswana, Ethiopia, Libya or Tanzania (42, 46, 58–62, 87, 93). S. chromogenes is a major cause of mastitis and subclinical mastitis in animals as seen in this review (21, 56, 57, 66, 75, 76, 84, 90, 106). However, no S. chromogenes infections were recorded in Botswana, Algeria, Ethiopia, Libya and Tanzania (42, 46, 58–62, 64, 70, 73, 87, 93, 120). The strain distribution could not be described due to the insufficient published data, but we were able to describe epidemiology of SOSA in terms of species distribution.
We observed that about 50% of the eligible studies utilized semi-automated methods (API-Staph and BD Phoenix) based on biochemical reactions. However, speciation of SOSA through these methods is unreliable as various species exhibit similar characteristics, hence molecular and spectrometric methods such as polymerase chain reaction (PCR) and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) have been advocated (121, 122). Investigators pay little attention to SOSA as they are often considered contaminants, leading to the lack of speciation and strain typing. Therefore, there is sparse genotyping data on members of the SOSA, and it is difficult to understand the clonal diversity of SOSA on the continent and we could not describe clonal relationships with human-associated isolates.
The use of antibiotics in animal production and its consequent impact on AMR is a major challenge globally, particularly in Africa (15, 123, 124). We observed high rates of penicillin (58%) and tetracycline (28%) resistance in SOSA generally. The high rates (≥50%) of lincosamide, macrolide, and methicillin resistance observed in M. sciuri are note-worthy. Genes mediating resistance to these antibiotics could be transferred via mobile genetic elements to pathogenic bacteria such as S. aureus, as has previously been described for the SCCmec element (125, 126). High resistance to aminoglycosides, macrolides, tetracyclines, and methicillin was also observed in SOSA species (15–89%) which are commonly encountered in human medicine, such as S. epidermidis, S. haemolyticus, S. hominis, S. intermedius, and S. pseudintermedius, which might be due to the overuse of clinical antibiotics, particularly penicillin and tetracycline, in veterinary medicine (15). This could result in empiric treatment failures in clinical settings since these antibiotics are commonly used in human medicine. This again highlights the need for policymakers to enforce regulations on the use of antibiotics in animal husbandry in Africa.
Resistance to last resort antibiotics such as linezolid was also reported. This raises the risk of antibiotic resistance transfer to commensal S. aureus in animals, in which low rates of resistance to methicillin and other antibiotics have generally been observed in Africa (0–3%) (39). Interactions at the human-animal interface also raise the risk of antibiotic resistance transfer to humans. Studies have demonstrated that SOSA are becoming more resistant than S. aureus in humans (127, 128), although rates of methicillin resistance across Africa vary widely, from 12 to over 80% (129). The lack of methicillin resistance detection seen in this review might be due to the challenges associated with using cefoxitin and oxacillin for methicillin resistance screening in SOSA as discussed by Yang et al. (130) and Humphries et al. (2). Although, mecA or PBP2a PCR detection is the gold standard for assessment of methicillin resistance in staphylococci, PBP2a phenotypic testing may be an efficient, labor- and cost-saving approach (130, 131). The uneven distribution of studies has made it difficult to compare antibiotic resistant rates across the different regions. Furthermore, the high rates of antibiotic resistance seen in carriage SOSA can be attributed to the small sample size and the differences in species distribution but needs to be investigated further.
The findings from this review revealed that the epidemiology of SOSA is described mainly in cows, with insufficient data on companion animals such as dogs and cats in Africa. The very heterogeneous nature of the livestock and companion animals sampled in different regions does make it difficult to draw firm conclusions about the geographic distribution of different species and AMR rates among SOSA. We suggest that other livestock and companion animals should be investigated in future studies to better understand the problem of AMR in animals on the continent. Studies in Eastern Africa are more focused on infected livestock. Ethiopia particularly is home to Africa's largest livestock population and human interaction with healthy livestock is more frequent (132). We recommend that research in this region focuses on healthy animals to help address the problem of zoonotic transmissions. There is also a lack of data particularly in Central and Western Africa. It is important that research in these regions of Africa is encouraged to help understand the burden of AMR in animals in Africa. Few studies performed strain typing and molecular screening of antibiotic resistance genes. With the decrease in the cost of next-generation sequencing, researchers in Africa should consider employing whole genome sequencing (WGS), which can also provide additional data such as resistance, virulence, pathogenicity, and genetic composition of the organism (133).
Many studies did not indicate the sample collection period, and there was inadequate longitudinal data, describing SOSA or AMR in specific countries or regions; for example, from West Africa only Nigeria reported on SOSA in animals. Therefore, it was not possible to stratify data which is a limitation of the review. However, findings from this review shows that SOSA species are becoming more resistant to antibiotics, and this requires immediate attention.
Data availability statement
The original contributions presented in the study are included in the article/Supplementary material, further inquiries can be directed to the corresponding author/s.
Author contributions
RO contributed to the conceptualization and design of the systematic review, performed literature searches, data extraction and synthesis, data interpretation, and wrote the manuscript. JN, ZM, AH, TM, and MS performed literature searches, data extraction and synthesis, and provided critical feedback on the manuscript. MN-F, AW, WZ, GR, AA, and AS contributed to the conceptualization and design of the systematic review and provided critical feedback on the manuscript. All authors contributed to the article and approved the submitted version.
Funding
This study was supported by the German Research Council (DFG) through grant ZI665/3-1 and the German Federal Ministry of Education and Research (BMBF) through grant number 01KI1727E.
Acknowledgments
Thanks to Dinah Seligsohn, National Veterinary Institute, Sweden for providing us additional data on speciation of SOSA from her publication (52).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fvets.2022.1059054/full#supplementary-material
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Keywords: Africa, animals, antibiotic resistance, coagulase-negative staphylococci, non-aureus staphylococci, Staphylococci other than S. aureus
Citation: Ocloo R, Nyasinga J, Munshi Z, Hamdy A, Marciniak T, Soundararajan M, Newton-Foot M, Ziebuhr W, Shittu A, Revathi G, Abouelfetouh A and Whitelaw A (2022) Epidemiology and antimicrobial resistance of staphylococci other than Staphylococcus aureus from domestic animals and livestock in Africa: a systematic review. Front. Vet. Sci. 9:1059054. doi: 10.3389/fvets.2022.1059054
Received: 30 September 2022; Accepted: 16 November 2022;
Published: 13 December 2022.
Edited by:
Faham Khamesipour, Shahid Beheshti University of Medical Sciences, IranReviewed by:
Newton Valerio Verbisck, Brazilian Agricultural Research Corporation (EMBRAPA), BrazilAmany Arafa, NRC, Egypt
Eligia Maria Szewczyk, Medical University of Lodz, Poland
Adriana Belas, Universidade Lusófona, Portugal
Copyright © 2022 Ocloo, Nyasinga, Munshi, Hamdy, Marciniak, Soundararajan, Newton-Foot, Ziebuhr, Shittu, Revathi, Abouelfetouh and Whitelaw. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Remous Ocloo, remous@sun.ac.za; remouso@gmail.com