Next Article in Journal
The Biology of Colicin M and Its Orthologs
Previous Article in Journal
Public Health Literacy, Knowledge, and Awareness Regarding Antibiotic Use and Antimicrobial Resistance during the COVID-19 Pandemic: A Cross-Sectional Study
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Antibiotics
Volume 10
Issue 9
10.3390/antibiotics10091108
antibiotics-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Prevalence and Characteristics of Staphylococcus aureus Associated with Meat and Meat Products in African Countries: A Review

by
Thembeka Thwala
1,
Evelyn Madoroba
1,
Albert Basson
1 and
Patrick Butaye
2,3,*
1
Department of Biochemistry and Microbiology, University of Zululand, Private Bag X1001, KwaDlangezwa 3886, South Africa
2
Department of Biosciences, Ross University School of Veterinary Medicine, West Farm, Saint Kitts and Nevis
3
Bacteriology and Avian Diseases, Department of Pathology, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium
*
Author to whom correspondence should be addressed.
Antibiotics 2021, 10(9), 1108; https://doi.org/10.3390/antibiotics10091108
Submission received: 3 August 2021 / Revised: 26 August 2021 / Accepted: 1 September 2021 / Published: 14 September 2021
Versions Notes

Abstract

:
Antimicrobial resistance has been increasing globally, which negatively affects food safety, veterinary, and human medicine. Ineffective antibiotics may cause treatment failure, which results in prolonged hospitalisation, increased mortality, and consequently, increased health care costs. Staphylococcus aureus causes a diverse range of infections including septicaemia and endocarditis. However, in food, it mainly causes food poisoning by the production of enterotoxins. With the discovery of methicillin-resistant S. aureus strains that have a separate reservoir in livestock animals, which were termed as livestock-associated methicillin-resistant S. aureus (LA-MRSA) in 2005, it became clear that animals may pose another health risk. Though LA-MRSA is mainly transferred by direct contact, food transmission cannot be excluded. While the current strains are not very pathogenic, mitigation is advisable, as they may acquire new virulence genes, becoming more pathogenic, and may transfer their resistance genes. Control of LA-MRSA poses significant problems, and only Norway has an active mitigation strategy. There is limited information about LA-MRSA, MRSA in general, and other S. aureus infections from African countries. In this review, we discuss the prevalence and characteristics of antimicrobial susceptible and resistant S. aureus (with a focus on MRSA) from meat and meat products in African countries and compare it to the situation in the rest of the world.

1. Introduction

The increase in antimicrobial-resistant zoonotic bacterial pathogens has become a significant public health challenge. There are diverse drivers of antimicrobial resistance, with the use of antimicrobial agents in food-producing animals as a major driver of resistance in animal bacteria [1]. Ineffective antimicrobials may cause treatment failure, which results in prolonged hospitalisation and increased mortality, and consequently, increased health care costs.
Staphylococcus aureus causes a diverse range of infections in humans. These include severe diseases such as septicaemia and endocarditis, which are frequently associated with high mortality if not treated properly [2]. This bacterium has been reported in the last few decades to be resistant to many of the available antimicrobial agents, and recently, it became resistant to one of the last lines of treatment daptomycin and linezolid [3,4]. However, the most common cause of nosocomial and community-associated staphylococcal infections is methicillin-resistant S. aureus (MRSA) [5].
S. aureus has been documented as one of the most significant causes of hospital-acquired infections in the past decades. It belongs to the ESKAPE group of bacteria (Enterococcus spp., S. aureus, Klebsiella spp., Acinetobacter baumannii, Pseudomonas aeruginosa, Enterobacter spp.), all of which have multi-drug resistant profiles [6]. S. aureus has been associated with a high rate of antimicrobial resistance in both hospitals and other environments such as community settings [7]. While there was a slight decrease in infections with MRSA in the US, Europe, Canada, and South Africa, in some regions such as sub-Saharan Africa, the trends increased [8]. This increase is a public health concern.
S. aureus acquired resistance to methicillin and most other beta-lactamase resistant beta-lactam antibiotics through the acquisition of the mec gene located on the staphylococcal cassette chromosome mec (SCCmec) element [5]. While the mecA gene is the most prevalent, mecC has been mainly associated with animals, and it has also been detected in human and environmental staphylococci [9]. The MRSA was first described in 1961, and this occurred soon after methicillin was used as the first line of treatment for penicillin-resistant S. aureus [10]. Since then, MRSA has been reported worldwide in hospitals and from the early 1990s in community settings. During the early 1990s, oxacillin, and later on cefoxitin, was preferred over methicillin for testing the staphylococci, but the abbreviation MRSA is still used for historical reasons [11]. The promoter of the mecA genes can have several mutations, which may contribute to the variation of oxacillin MICs [12]. Some S. aureus strains may even be susceptible to oxacillin in vitro while simultaneously harbouring mecA, and they are referred to as OS-MRSAs [13]. OS-MRSAs have been associated with food, animals, and clinical strains and are important as causative agents of clinical challenges, as they may acquire resistance to β-lactams effortlessly [13]. Livestock-associated methicillin-resistant S. aureus (LA-MRSA) was only detected in 2005 and was found mainly amongst pigs and veal calves [9].
Contamination of food by S. aureus results from poor hygiene practices during food processing and storage. Both human- and animal-associated strains can be involved [14]. However, the strains that produce staphylococcal enterotoxins and mainly the staphylococcal enterotoxin A (SEA), encoded by the sea gene, cause food poisoning outbreaks [15]. The other toxins that may be involved are encoded by the seb, sec, sed and see enterotoxin genes [16].
Food poisoning by the staphylococcal toxin is characterised by diarrhoea, nausea, abdominal cramping, and vomiting within 24 h of ingestion [17]. However, with the advent of LA-MRSA, other health risks than food poisoning should be considered. Different studies have indicated that LA-MRSA (and other types of MRSA) can be present in milk, poultry, cattle, pigs, and pets [14,17,18,19,20,21]. In Europe, the most prevalent LA-MRSA clonal complex is CC398; however, other lineages such as ST1, ST5, ST9, ST97, ST130, and ST433 have been reported. In Asia, the majority of the strains belong to CC9, while in North America, CC398 and CC9 were equally common [21]. Though LA-MRSA is mainly transferred by direct contact, food transmission cannot be excluded. While the current strains are not very pathogenic, mitigation strategies are advisable, as these bacteria may acquire new virulence genes and become more pathogenic [9]. Moreover, the transfer of resistance genes should also be taken into account.
There is limited information about MRSA, LA-MRSA, and other S. aureus infections from African countries. In this review, we discuss the prevalence and characteristics of S. aureus, including MRSA recovered from meat and meat products in African countries, and evaluate the extent of antimicrobial resistance of S. aureus recovered from humans and animals in African countries, compared to other regions.

2. The Prevalence of S. aureus in Meat and Meat Products in African Countries

Animals such as cattle, pigs, chickens, turkey, horses, sheep, and man can be colonised by S. aureus on their skin and in their nares [22]. Typically, different clones are associated with specific hosts, though some clones lack host specificity while others can occasionally infect other species [23]. Few studies in Africa have described S. aureus in meat and meat products. Moreover, few isolates have been characterized in detail. Different types of meat may have a different prevalence and, in this section, we handle the different meat types separately.

2.1. Prevalence of S. aureus in Raw Unprocessed Red Meat

In Table 1, a summary of the studies performed on raw unprocessed red meat in Africa is listed.
We could find data on a total of 2853 samples from all over Africa. Overall, 699 were contaminated with S. aureus. Positive samples included raw unprocessed beef, pork, goat meat, camel meat, lamb/sheep, and unspecified red meat products. The total prevalence of S. aureus in meat products was 24.5%, and of all red meats, beef samples showed the highest prevalence with 33.08% of the samples being positive. These findings indicate a higher potential risk of beef for human infections. Compared to data from other countries, the results are similar [36,37,38,39], though in China, a higher percentage of contamination was found, with a little over 50% of the raw beef samples found positive [40], as well as in a specific study from the US where a prevalence of 65.6% was found in retail beef [14], while in another US study, the overall positivity S. aureus was 16.4% [41]. This large variation in both Africa and worldwide may be attributed to several factors, including sampling method, isolation methods, sampling site on the carcass, different cuts of meat, contamination during and after the slaughter, storage of the meat, as well as the processing of the meat [42]. A total of 691 pork samples were analysed in Africa (Table 1), and almost 14% of them were found positive for S. aureus. These findings are similar to what was found in the US [38], while much higher percentages were found in other studies from the US and Brazil [39,43,44,45]. In Asia, a lower prevalence was found [40].
There was quite some variation in the prevalence between the African countries, even between studies from the same country as exemplified by the Nigerian studies. In Nigeria, there was an apparent increase in prevalence [27,46], and the reasons for this apparent increase remain unclear. In South Africa, two studies performed in the same year showed also substantial differences [25,26]. However, the studies used a different type of sample and a different way of collecting the sample, different isolation methods, and were conducted in a different geographical location. In Ivory Coast, similar to beef, the prevalence was lowest [24]. Additionally, here it is clear that the few data available do not allow a broad conclusion on the prevalence nor evolution of the contamination of meat products in Africa. Hence, it is necessary to conduct more research on the subject in Africa.
Only one study reported the prevalence of S. aureus from goat meat [27]. The prevalence was on the lower side. Similarly, only two studies were conducted on the prevalence of S. aureus in sheep meat. Both were conducted in South Africa, and the results showed major differences [25,26]. Only Egypt reported the prevalence of S. aureus from camel meat [32]. Those studies do not allow to have a good view on the prevalence of S. aureus in those meats; however, it indicates that also those meat products can substantially be contaminated. Surprisingly, on unspecified raw red meat in Nigeria, nearly all products were contaminated [34], while a former study showed a low level of contamination [33].
The distribution of Staphylococcus aureus in red meat differs, thus widely based on different studies, and it seems to be dependent on both the country and the meat product, though other factors cannot be excluded. No firm conclusion on differences between countries, in time or red meat type, can be made, as the studies are too limited and too different. It is, however, clear that S. aureus contamination of red meat products is, and remains, a problem that needs mitigation.

2.2. Prevalence of S. aureus in Raw Unprocessed Poultry

Compared to red meats, quite a lot more samples from poultry have been analysed, though the numbers are still limited relative to the vastness of the African continent. Moreover, the studies have been performed in a limited number of counties (Table 2). We could find data from 11,080 samples of chicken meat, and of those, a little over 20% were found to be contaminated with S. aureus (Table 2). The prevalence of S. aureus in poultry meat seems to be lower than in beef. The oldest study is from Nigeria and was performed in 2009 on a relatively small number of samples. The prevalence was very high, with 80% of the samples being positive [27]. A second larger study performed in 2011 from Tunisia showed, however, only 51.19% of the samples were positive [47]. Due to differences in sample size, it is difficult to assess whether there was a potential evolution. Similarly, in South Africa, the prevalence seems to drop over time, but it remained a high prevalence [25,26]. Other studies in African countries were limited, though one very large study in Algeria showed a prevalence of close to 20%, which is close to the average prevalence measured for all of Africa [28].
The overall prevalence found in Africa is similar to what has been found in China and Brazil [45,48]. In the US, a higher prevalence was found in most of the studies, though one study showed a prevalence as low as 0.3% [39,43,49]. There are few data available from Asiatic countries, and the prevalence rates were overall lower than in most other countries [48,50]; however, a conflicting study reported a higher prevalence of 70% [20]. From the data published, it is clear that poultry in Africa is also contaminated with S. aureus, though to a lesser extent than most other studies.

2.3. Prevalence of S. aureus in Raw Processed Meat

Table 3 shows the studies that have determined the prevalence of S. aureus in raw processed meats. All were beef samples. Out of 247 tested samples, 31 (13%) were positive for S. aureus. One would expect higher levels of contamination, compared to unprocessed meat, as processed meat is more prone to microbial contamination. However, we could not confirm this with the published data. It should be noted also that some processes such as smoking and drying may reduce contamination, and from the above studies, the meat used was dried and smoked. As no ample data are present, no real conclusions can be drawn for this type of food.

2.4. Prevalence of S. aureus in Ready-to-Eat Meat

Table 4 indicates the prevalence of S. aureus from ready-to-eat meat, and only one study was found and few samples were included. This study showed a low prevalence of S. aureus.
The contamination of meat by S. aureus across the food chain is a complicated process. The contamination may originate from animals, as well as from humans. It has been shown before that in humans, the main source of contamination is food handlers that carry S. aureus in their noses or hands [54]. Improper hygiene at that level should be avoided to reduce the odds of meat contamination and food poisoning. However, due to the multitude of small slaughter and meat processing operations in Africa, this may prove to be difficult.
The other source of contamination is the animals themselves. Food-producing animals carry S. aureus on their skin, nose, as well as in their intestine. The main factors that influence the level of contamination are the length at which animals are transported and the methods which are used to move animals from one place to another, holding conditions, geographic location, as well as climate changes [55]. Next to that, it is always important to follow proper slaughter and food handling protocols to minimise contamination with pathogenic microorganisms. The growth of S. aureus and the production of enterotoxins in food is caused by improper handling of foods and the improper storage conditions that support the growth of this pathogen [56]. In developing countries, pathogens are being transmitted from livestock to humans through contact or contaminated meat or meat products [57]. Only typing of the strains can bring clarity in the origin of the contamination and the public health risk associated with the contamination.
In Africa, red meat has the highest prevalence of S. aureus, compared to other types of meat. S. aureus has been reported to be one of the pathogens causing foodborne infections from different regions worldwide. Findings indicate a specific problem on the African continent in beef production that needs further investigation.
Few studies in Africa have assessed contamination sites across the food chain. However, in Ethiopia, S. aureus was found on all equipment that was used in the abattoirs [58].
From the results obtained in our review, more research needs to be conducted in Africa to fully understand the prevalence and way of spread of S. aureus via the food chain. It is also important that African countries should improve the hygiene conditions, especially in abattoirs, butcheries, and retail shops to improve public health. S. aureus has been associated with foodborne diseases in different parts of the world, and infections caused by this pathogen are difficult to treat because some strains are resistant to antibiotics.

3. Antimicrobial Resistance in S. aureus from Meat and Meat Products in Africa

The data for antimicrobial resistance in different types of meat from various African countries comprised 20 antibiotics that were tested, representing 10 different classes of antibiotics (Table 5). Not all studies used the same antibiotics, hence the difference in the number of strains tested. Studies originated from Nigeria, South Africa, Cameroon, Algeria, Tunisia, and Egypt, and the cumulated results are represented in Table 5. Due to the limited number of studies and the limited number of strains involved, few conclusions can be drawn on differences between regions. Nevertheless, an overall view may help in what antimicrobial resistance is present in Africa. Due to the differences in the numbers of strains tested, the resistance percentages within an antibiotic class may vary. Therefore, the data presented only give an impression of the resistance problem.
High resistance was observed from ampicillin (50%), clindamycin (33.8%), doxycycline (27%), and ofloxacin (57%), though ofloxacin represented a small sample size.
Upon examination of the data in more detail, we observe that the resistance against beta-lactam antibiotics is in general quite high. It is surprising to see such high resistance against the penicillinase-resistant β-lactam antibiotics, as the isolation methods that were used were not specifically targeting MRSA. It should be noted, however, that in the concerned studies, the resistance was not confirmed by PCR and may thus be lower [28,32,34,54,59]. Nevertheless, it is an indication that the levels of MRSA on meat samples may be quite high. It has indeed been shown that meat can be contaminated by LA-MRSA, especially pork, as the prevalence of LA-MRSA is high in pigs, as well as by human MRSA strains [60]. Nevertheless, MRSA should be confirmed by PCR, as the disk diffusion test is not very accurate for the determination of MRSA [61]. Thus, the true prevalence of MRSA in meat remains obscure. Interestingly, one group tested for ceftaroline, an anti-MRSA antibiotic, and the resistance is high [26]. Vancomycin (0.7%) and gentamicin (1%) showed very low resistance, and only against amikacin, there was quite some resistance. Resistance against vancomycin in S. aureus, as determined by the disk diffusion test, is not very reliable [62], and the presence of vancomycin resistance in S. aureus may thus be questionable. Resistance against the tetracyclines is somewhat varying between studies, as was the case with the difference in the prevalence of resistance against the different antibiotics in this class. A similar observation can be made for fluoroquinolones. Resistance against other antibiotics was medium to low. Apart from the presence of MRSA, there does not seem to be a very large problem with resistance in this bacterium on meat and meat products in Africa.
Compared to other parts in the world where antimicrobial resistance has been assessed on strains from food, similar resistance percentages were noted such as in China, [63,64], the USA [39], Greece [65], India [66], Italy [37,67,68]. Few other studies showed differences, including a German study, which showed high resistance in tetracycline, oxacillin, erythromycin, clindamycin, kanamycin, gentamicin, and ciprofloxacin in S. aureus from turkey meat [69].

4. Antimicrobial Resistance Genes Detected in S. aureus from Meat in Africa

Only two studies reported the resistance genes present in S. aureus (MSSA) from meat products in Africa (Table 6). The genes identified are commonly identified worldwide [76]. However, since the data come only from two countries, with each one being a limited study (Table 6), conclusions are difficult to make.

5. Genotyping of Different S. aureus Meat Isolates from Africa

The genetic background of only a few strains has been determined, and all came from a single study in Tunisia (Table 7) [47]. Four strains were MSSA ST398, which is surprising as most ST398 strains are MRSA and came from chicken and veal. MSSA CC398 has been mainly associated with humans [77], where the human evasion cluster genes IEC are, in general, present [78]. Other clonal complexes detected included ST22 which is also mainly associated with human infections [79], though it has also been associated with infections in animals including outbreaks in veterinary clinics [80,81,82]. The ST8 clone is a typical community-acquired clone also associated with hospital outbreaks, usually being an MRSA as the USA300 clone [83], which has been reported worldwide, including sub-Saharan Africa [84,85]. The presence of MSSA ST398, ST8, and ST22 indicates that they might be more associated with humans contaminating the meat, either during slaughter, processing, or storage.

6. MRSA in Meat Products in Africa

6.1. Prevalence and Characteristics of Methicillin-Resistant S. aureus (MRSA) in Different Types of Meat

We separated the studies dealing with the detection of MRSA from the other studies, as they applied a very different methodology. Using selective isolation, the studies were focusing only on the presence of a specific subtype of S. aureus and thus not giving a full picture of the presence of S. aureus. Moreover, these MRSA have never been implicated in food poisoning and have thus a more zoonotic aspect. These strains can be of animal origin (the LA-MRSA) or they can originate from humans. The LA-MRSA are specific types of MRSA that can be distinguished by molecular typing. Therefore, the prevalence of LA-MRSA is mainly related to carcass contamination from animal origin, rather than other origins. Therefore, the prevalence of LA-MRSA is in direct relation with the prevalence in the animal itself, although not excluding cross-contamination during slaughter and processing.
We found data on the selective isolation of MRSA from a total of 3746 meat samples which included beef, pork, and poultry (Table 8). The numbers should be interpreted with care, however, as not all MRSA cases were confirmed, and false-positive results are possible. This is also evident in Table 6, where not all strains are resistant to all β-lactam antibiotics. The highest prevalence of MRSA was observed in pork (12%), which is the animal species with the highest prevalence of LA-MRSA worldwide. However, the carriage differs across the countries, and the prevalence at pig meat level is, in general, lower than the prevalence at farm level [86]. The prevalence rates in poultry and beef were 6.76% and 6.12%, respectively. The prevalence of LA-MRSA in these latter species has been shown to be lower than in pigs except for veal calves [86]. The prevalence of MRSA in pork in Africa is, however, much lower, compared to what has been found in countries with a high prevalence of LA-MRSA in pigs [45,67,87,88,89]. More research is required in order to determine whether the prevalence of LA-MRSA in animals is indeed lower in Africa. Nevertheless, the prevalence of MRSA in pork from countries such as China and the USA, where the prevalence in pigs is moderate to high, was lower [36,41,43,64]. The prevalence of MRSA in chicken meat from Africa (6.76%) was lower or similar, compared to most other studies [20,41,45,48,64,90,91].
Prevalence in beef was 6.12%, which was higher than 4%, 0.8%, and 1.7% found in beef meat from the USA [36,38,49] and also 4.4% found in Hong Kong [91], while in Brazil, a very high prevalence (23.3%) was found [45]. However, more research is required in order to ascertain the extent of MRSA contamination of meat in Africa.

6.2. Antimicrobial Resistance Profile of MRSA in African Countries

From Table 9, it is clear that not all tests were performed accurately, as MRSA is resistant to all beta-lactam antibiotics that were included in testing (there were no anti-MRSA β-lactams included). Nevertheless, several strains were not confirmed by PCR to be MRSA, which might affect the final results. Resistance was commonly found against tetracyclines, which is indicative of the presence of LA-MRSA ST398. These strains are classically nearly 100% resistant to tetracyclines. LA-MRSA is also typically multidrug resistant, with high resistance percentages against aminoglycosides, macrolides, and lincosamides, as well as fluoroquinolones, though this may vary a bit according to the studies [88,94,95,96,97]. Thus, the data strongly indicate that many MRSA could be LA-MRSA. The high prevalence of vancomycin resistance has to be interpreted with care, as the studies were carried out using the disk diffusion test, and this is not very reliable [98,99]. Vancomycin resistance has never been reported before in LA-MRSA and is extremely rare in other MRSA.
Unfortunately, there are little data from Africa on the prevalence of LA-MRSA [42], though it is present in animals. It has indeed been shown that meat can be contaminated by LA-MRSA, especially pork since the prevalence of LA-MRSA is, in general, highest in pigs [60]. Nevertheless, MRSA should be confirmed by PCR, as the disk diffusion test is not very accurate for the determination of MRSA [61]. The true prevalence of MRSA in meat remains thus unclear.

7. Antimicrobial Resistance Genes Detected in MRSA from Meat in Africa

In few studies, a selection of resistance genes in MRSA have been determined, which makes the data rather incomplete (Table 10). The genes found in Africa are the classical genes found worldwide, though one big exception is the presence of vanA and vanB in Egyptian camel and beef isolates [30,32]. Vancomycin resistance mediated by the vanA or vanB gene in staphylococci has rarely been described in staphylococci and is mainly associated with vancomycin resistance in enterococci [10]. The reason for this presence of vancomycin could be the use of avoparcin, another glycopeptide antibiotic, which is frequently used in Egypt for the prevention of necrotic enteritis and as a growth promoter in the poultry industry [100]. Another description of vancomycin resistance in Egypt was from ready-to-eat food (beef burgers and hot dogs); however, in these four strains, no van gene-mediated resistance could be detected [101]. Unfortunately, these strains have not been typed, and therefore, it is unclear whether these might be strains of human or animal origin. A survey conducted from Egypt hospital on dairy food, food handlers, and patients indicated the presence of methicillin-resistant, coagulase-positive, and vancomycin-resistant staphylococci but only from humans (food handlers and patients) [102], whereas coagulase-negative staphylococci (both MR and VR) were identified from food, food handlers, and patients; however, antimicrobial resistance genes were not studied [102]. Hospital infections with VRSA have been described on occasions in Egypt [103]. The presence of vancomycin resistance in MRSA is highly concerning, as it renders an infection with these bacteria very hard to treat. The situation seems unique to Egypt.

8. Genotyping of MRSA Meat Isolates from Africa

In South Africa, ST612 (a CC8 strain) has been associated with human infections and has been identified as a dominant clone in hospitals in Cape Town and other provinces [71,104]. However, this clone has also been frequently isolated from animals in other continents such as horses in Australia [105], leading to the detection of the strains also in veterinarians working with horses and other people in contact with horses [67,106,107,108], which indicates the possible transmission from humans to animals. This clone was also multidrug resistant, hence the importance of its spread through the food chain [109].
The presence of ST398 (CC398) indicates that the situation in North Africa might be more similar to Europe, as this is the most detected LA-MRSA clone in animals. Probably this is due to its closer geographical location. The ST398 clonal complex is associated with multi-resistance, including heavy metal resistance, which highlights the need for more studies in Africa on its prevalence. There is thus a need for more research on the prevalence and characteristics of LA-MRSA in African countries [29].
The current data are not representative of what types of MRSA can be found in meat from Africa, nor even of the two countries on which we have information regarding typed strains. The typed MRSA isolates are derived from a single study in Tunisia and two studies from South Africa (Table 11) [47,71,110]. Only in the study by Chairat, typical LA-MRSA ST398 were detected, next to an ST30 strain, which is known to be human associated [47]. In South Africa, one ST239 was found, which is peculiar, as ST239 has been found in animals only on rare occasions and only in Belgium [111,112,113]. ST239 has been mainly reported as an MRSA clone spreading in Asia, though it has also been detected in South Africa and other African countries [114,115,116,117]. It is thus not clear whether this strain might be of animal or human origin, as there are not enough data on the types of MRSA in animals in South Africa.

9. Conclusions

Unfortunately, there is little information on S. aureus from meat products in Africa, and there is even less on the types and their antimicrobial resistance. Nevertheless, the observation is that meats can be heavily contaminated with S. aureus, including MRSA, and this represents a potential public health threat. There is thus an urgent need for more studies on the subject to be able to estimate the public health burden. The current studies are fragmentary using different methodologies, which makes it difficult to compare studies. While the MRSA clones on meat detected in few studies seem to be mainly of human origin, the presence of LA-MRSA CC398 warrants further investigation, as does the presence of VISA.

Author Contributions

Conceptualisation, E.M. and P.B.; writing—original draft preparation, T.T.; writing—review and editing, P.B., E.M. and A.B.; supervision, P.B., E.M. and A.B.; project administration, E.M.; funding acquisition, E.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Red Meat Research and Development Trust-South Africa (RMRDSA) and the Department of Trade and Industry-Technology and Human Resources for Industry Programme (DTI-THRIP), Grant Number THRIP/22/30/11/2017.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors express gratitude to Sidney Maliehe for assisting the first author with formatting the manuscript.

Conflicts of Interest

The authors declare no conflict of interest. The fundrs had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Devkota, S.P.; Joshi, L.R. Methicillin-Resistant Staphylococcus aureus (MRSA) in Cattle: Epidemiology and Zoonotic Implications. Int. J. Appl. Sci. Biotechnol. 2014, 2, 29–33. [Google Scholar]
  2. Alfatemi, S.M.H.; Motamedifar, M.; Hadi, N.; Saraie, H.S.E. Analysis of Virulence Genes Among Methicillin Resistant Staphylococcus aureus (MRSA) Strains. Jundishapur. J. Microbiol. 2014, 7, e10741. [Google Scholar] [CrossRef] [Green Version]
  3. Markwart, R.; Willrich, N.; Eckmanns, T.; Werner, G.; Ayobami, O.J.F. Low proportion of linezolid and daptomycin resistance among bloodborne vancomycin-resistant Enterococcus faecium and methicillin-resistant Staphylococcus aureus infections in Europe. Front. Microbiol. 2021, 12, 664199. [Google Scholar] [CrossRef]
  4. Jones, C.H.; Tuckman, M.; Howe, A.Y.; Orlowski, M.; Mullen, S.; Chan, K.; Bradford, P.A. Diagnostic PCR analysis of the occurrence of methicillin and tetracycline resistance genes among Staphylococcus aureus isolates from phase 3 clinical trials of tigecycline for complicated skin and skin structure infections. Antimicrob. Agents Chemother. 2006, 50, 505–510. [Google Scholar] [CrossRef] [Green Version]
  5. Li, J.; Jiang, N.; Ke, Y.; Fessler, A.T.; Wang, Y.; Schwarz, S.; Wu, C. Characterization of pig-associated methicillin-resistant Staphylococcus aureus. Vet. Microbiol. 2017, 201, 183–187. [Google Scholar] [CrossRef] [PubMed]
  6. Pendleton, J.N.; Gorman, S.P.; Gilmore, B.F. Clinical relevance of the ESKAPE pathogens. Expert Rev. Anti-Infect. Ther. 2013, 11, 297–308. [Google Scholar] [CrossRef] [PubMed]
  7. Chambers, H.F.; Deleo, F.R. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 2009, 7, 629–641. [Google Scholar] [CrossRef]
  8. Chaudhary, A.S. A review of global initiatives to fight antibiotic resistance and recent antibiotics discovery. Acta Pharm. Sin. B 2016, 6, 552–556. [Google Scholar] [CrossRef] [Green Version]
  9. Butaye, P.; Argudín, M.A.; Smith, T.C. Livestock-Associated MRSA and Its Current Evolution. Curr. Clin. Microbiol. Rep. 2016, 3, 19–31. [Google Scholar] [CrossRef] [Green Version]
  10. Lowy, F.D. Antimicrobial resistance: The example of Staphylococcus aureus. J. Clin. Investig. 2003, 111, 1265–1273. [Google Scholar] [CrossRef]
  11. Lee, J.H. Methicillin (Oxacillin)-Resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Appl. Environ. Microbiol. 2003, 69, 6489–6494. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Chen, F.-J.; Wang, C.-H.; Chen, C.-Y.; Hsu, Y.-C.; Wang, K.-T. Role of the mecA gene in oxacillin resistance in a Staphylococcus aureus clinical strain with a pvl-positive ST59 genetic background. Antimicrob. Agents Chemot. 2014, 58, 1047–1054. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Boonsiri, T.; Watanabe, S.; Tan, X.-E.; Thitiananpakorn, K.; Narimatsu, R.; Sasaki, K.; Takenouchi, R.; Sato’o, Y.; Aiba, Y.; Kiga, K.; et al. Identification and characterization of mutations responsible for the β-lactam resistance in oxacillin-susceptible mecA-positive Staphylococcus aureus. Sci. Rep. 2020, 10, 16907. [Google Scholar] [CrossRef] [PubMed]
  14. Abdalrahman, L.S.; Wells, H.; Fakhr, M.K. Staphylococcus aureus is More Prevalent in Retail Beef Livers than in Pork and other Beef Cuts. Pathogens 2015, 4, 182–198. [Google Scholar] [CrossRef] [Green Version]
  15. Hennekinne, J.A.; De Buyser, M.L.; Dragacci, S. Staphylococcus aureus and its food poisoning toxins: Characterization and outbreak investigation. FEMS Microbiol. Rev. 2012, 36, 815–836. [Google Scholar] [CrossRef] [Green Version]
  16. Omwenga, I.; Aboge, G.O.; Mitema, E.S.; Obiero, G.; Ngaywa, C.; Ngwili, N.; Wamwere, G.; Wainaina, M.; Bett, B. Staphylococcus aureus enterotoxin genes detected in milk from various livestock species in northern pastoral region of Kenya. Food Control 2019, 103, 126–132. [Google Scholar] [CrossRef]
  17. Abdalrahman, L.S.; Fakhr, M.K. Incidence, Antimicrobial Susceptibility, and Toxin Genes Possession Screening of Staphylococcus aureus in Retail Chicken Livers and Gizzards. Foods 2015, 4, 115–129. [Google Scholar] [CrossRef] [Green Version]
  18. Abdel-Hameid Ahmed, A.; Saad Maharik, N.M.; Valero, A.; Kamal, S.M. Incidence of enterotoxigenic Staphylococcus aureus in milk and Egyptian artisanal dairy products. Food Control 2019, 104, 20–27. [Google Scholar] [CrossRef]
  19. Ahmadi, M.; Rohani, S.M.R.; Ayremlou, N. Detection of Staphylococcus aureus in milk by PCR. Comp. Clin. Pathol. 2009, 19, 91–94. [Google Scholar] [CrossRef]
  20. Ali, Y.; Islam, M.A.; Muzahid, N.H.; Sikder, M.O.F.; Hossain, M.A.; Marzan, L.W. Characterization, prevalence and antibiogram study of Staphylococcus aureus in poultry. Asian Pac. J. Trop. Biomed. 2017, 7, 253–256. [Google Scholar] [CrossRef]
  21. Feltrin, F.; Alba, P.; Kraushaar, B.; Ianzano, A.; Argudin, M.A.; Di Matteo, P.; Porrero, M.C.; Aarestrup, F.M.; Butaye, P.; Franco, A.; et al. A Livestock-Associated, Multidrug-Resistant, Methicillin-Resistant Staphylococcus aureus Clonal Complex 97 Lineage Spreading in Dairy Cattle and Pigs in Italy. Appl. Environ. Microbiol. 2016, 82, 816–821. [Google Scholar] [CrossRef] [Green Version]
  22. Fo, O.; Pa, A.; Ob, K.; Oa, O. Prevalence and Antibiogram of Methicilin-Susceptible Staphylococcus aureus (MSSA) Isolated from Raw Milk of Asymptomatic Cows In Abeokuta, Nigeria. Alex. J. Vet. Sci. 2018, 59, 34. [Google Scholar] [CrossRef]
  23. Matuszewska, M.; Murray, G.G.; Harrison, E.M.; Holmes, M.A.; Weinert, L.A. The evolutionary genomics of host specificity in Staphylococcus aureus. Trends Microbiol. 2020, 28, 465–477. [Google Scholar] [CrossRef]
  24. Attien, P.; Sina, H.; Moussaoui, W.; Dadieacute, T.; Chabi, S.K.; Djeacuteni, T.; Bankole, H.S.; Kotchoni, S.O.; Edoh, V.; Prévost, G.; et al. Prevalence and antibiotic resistance of Staphylococcus strains isolated from meat products sold in Abidjan streets (Ivory Coast). Afr. J. Microbiol. Res. 2013, 7, 3285–3293. [Google Scholar] [CrossRef] [Green Version]
  25. Jaja, I.F.; Green, E.; Muchenje, V. Aerobic mesophilic, coliform, Escherichia coli, and Staphylococcus aureus counts of raw meat from the formal and informal meat sectors in South Africa. Int. J. Environ. Res. Public Health 2018, 15, 819. [Google Scholar] [CrossRef] [Green Version]
  26. Pekana, A.; Green, E. Antimicrobial resistance profiles of Staphylococcus aureus isolated from meat carcasses and bovine milk in abattoirs and dairy farms of the Eastern Cape, South Africa. Int. J. Environ. Res. Public Health 2018, 15, 2223. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Adesiji, Y.; Alli, O.; Adekanle, M.; Jolayemi, J. Prevalence of Arcobacter, Escherichia coli, Staphylococcus aureus and Salmonella species in retail raw chicken, pork, beef and goat meat in Osogbo, Nigeria. Sierra Leone J. Biomed. Res. 2011, 3, 8–12. [Google Scholar] [CrossRef] [Green Version]
  28. Bounar-Kechih, S.; Taha Hamdi, M.; Aggad, H.; Meguenni, N.; Cantekin, Z. Carriage methicillin-resistant Staphylococcus aureus in poultry and cattle in Northern Algeria. Vet. Med. Int. 2018, 2018, 4636121. [Google Scholar] [CrossRef] [Green Version]
  29. Osman, K.M.; Amer, A.M.; Badr, J.M.; Saad, A.S. Prevalence and antimicrobial resistance profile of Staphylococcus species in chicken and beef raw meat in Egypt. Foodborne Pathog. Dis. 2015, 12, 406–413. [Google Scholar] [CrossRef]
  30. El Tawab, A.A.A.; Maarouf, A.A.; El-Rais, E.M. Bacteriological and molecular studies on antibiotic resistant Staphylococcus aureus isolated from meat and its products in Qaliobaya, Egypt. Benha Vet. Med J. 2018, 34, 360–373. [Google Scholar]
  31. Morcillo, A.; Castro, B.; Rodríguez-Álvarez, C.; Abreu, R.; Aguirre-Jaime, A.; Arias, A. Descriptive analysis of antibiotic-resistant patterns of methicillin-resistant Staphylococcus aureus (MRSA) st398 isolated from healthy swine. Int. J. Environ. Res. Public Health 2015, 12, 611–622. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Al-Amery, K.; Elhariri, M.; Elsayed, A.; El-Moghazy, G.; Elhelw, R.; El-Mahallawy, H.; El Hariri, M.; Hamza, D. Vancomycin-resistant Staphylococcus aureus isolated from camel meat and slaughterhouse workers in Egypt. Antimicrob. Resist. Infect. Control 2019, 8, 129. [Google Scholar] [CrossRef] [Green Version]
  33. Ndahi, M.D.; Kwaga, J.K.; Bello, M.; Kabir, J.; Umoh, V.J.; Yakubu, S.E.; Nok, A.J. Prevalence and antimicrobial susceptibility of Listeria monocytogenes and methicillin-resistant Staphylococcus aureus strains from raw meat and meat products in Zaria, Nigeria. Lett. Appl. Microbiol. 2014, 58, 262–269. [Google Scholar] [CrossRef] [PubMed]
  34. Akagha, T.; Gugu, T.; Enemor, E.; Ejikeugwu, P.; Ugwu, B.; Ugwu, M. Prevalence and antibiogram of Salmonella species and Staphylococcus aureus in retail meats sold in Awka metropolis, southeast Nigeria. Int. J. Biol. Pharm. Res. 2015, 6, 924–929. [Google Scholar]
  35. Norman, G.R.; Streiner, D.L. Biostatistics: The Bare Essentials, 4th ed.; People’s Medical Publishing House-USA: Shelton, CT, USA, 2014. [Google Scholar]
  36. Jackson, C.R.; Davis, J.A.; Barrett, J.B. Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. J. Clin. Microbiol. 2013, 51, 1199–1207. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Pesavento, G.; Ducci, B.; Comodo, N.; Nostro, A.L. Antimicrobial resistance profile of Staphylococcus aureus isolated from raw meat: A research for methicillin resistant Staphylococcus aureus (MRSA). Food Control 2007, 18, 196–200. [Google Scholar] [CrossRef]
  38. Pu, S.; Han, F.; Ge, B. Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl. Environ. Microbiol. 2009, 75, 265–267. [Google Scholar] [CrossRef] [Green Version]
  39. Waters, A.E.; Contente-Cuomo, T.; Buchhagen, J.; Liu, C.M.; Watson, L.; Pearce, K.; Foster, J.T.; Bowers, J.; Driebe, E.M.; Engelthaler, D.M.; et al. Multidrug-Resistant Staphylococcus aureus in US Meat and Poultry. Clin. Infect. Dis. 2011, 52, 1227–1230. [Google Scholar] [CrossRef]
  40. Wu, S.; Huang, J.; Wu, Q.; Zhang, J.; Zhang, F.; Yang, X.; Wu, H.; Zeng, H.; Chen, M.; Ding, Y.; et al. Staphylococcus aureus Isolated From Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity. Front. Microbiol. 2018, 9, 2767. [Google Scholar] [CrossRef]
  41. Hanson, B.M.; Dressler, A.E.; Harper, A.L.; Scheibel, R.P.; Wardyn, S.E.; Roberts, L.K.; Kroeger, J.S.; Smith, T.C. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J. Infect. Public Health 2011, 4, 169–174. [Google Scholar] [CrossRef] [Green Version]
  42. Lozano, C.; Gharsa, H.; Ben Slama, K.; Zarazaga, M.; Torres, C. Staphylococcus aureus in Animals and Food: Methicillin Resistance, Prevalence and Population Structure. A Review in the African Continent. Microorganisms 2016, 4, 12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Buyukcangaz, E.; Velasco, V.; Sherwood, J.S.; Stepan, R.M.; Koslofsky, R.J.; Logue, C.M. Molecular typing of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) isolated from animals and retail meat in North Dakota, United States. Foodborne Pathog. Dis. 2013, 10, 608–617. [Google Scholar] [CrossRef]
  44. Abdalrahman, L.S.; Stanley, A.; Wells, H.; Fakhr, M.K. Isolation, Virulence, and Antimicrobial Resistance of Methicillin-Resistant Staphylococcus aureus (MRSA) and Methicillin Sensitive Staphylococcus aureus (MSSA) Strains from Oklahoma Retail Poultry Meats. Int. J. Environ. Res. Public Health 2015, 12, 6148–6161. [Google Scholar] [CrossRef] [PubMed]
  45. Costa, W.L.; Ferreira, J.D.S.; Carvalho, J.S.; Cerqueira, E.S.; Oliveira, L.C.; Almeida, R.C. Methicillin-resistant Staphylococcus aureus in raw meats and prepared foods in public hospitals in salvador, Bahia, Brazil. J. Food Sci. 2015, 80, M147-50. [Google Scholar] [CrossRef] [PubMed]
  46. Igbinosa, E.O.; Beshiru, A.; Akporehe, L.U.; Oviasogie, F.E.; Igbinosa, O.O. Prevalence of methicillin-resistant Staphylococcus aureus and other Staphylococcus species in raw meat samples intended for human consumption in Benin City, Nigeria: Implications for Public Health. Int. J. Environ. Res. Public Health 2016, 13, 949. [Google Scholar] [CrossRef]
  47. Chairat, S.; Gharsa, H.; Lozano, C.; Gomez-Sanz, E.; Gomez, P.; Zarazaga, M.; Boudabous, A.; Torres, C.; Ben Slama, K. Characterization of Staphylococcus aureus from Raw Meat Samples in Tunisia: Detection of Clonal Lineage ST398 from the African Continent. Foodborne Pathog. Dis. 2015, 12, 686–692. [Google Scholar] [CrossRef]
  48. Wang, X.; Tao, X.; Xia, X.; Yang, B.; Xi, M.; Meng, J.; Zhang, J.; Xu, B. Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in retail raw chicken in China. Food Control 2013, 29, 103–106. [Google Scholar] [CrossRef]
  49. Ge, B.; Mukherjee, S.; Hsu, C.-H.; Davis, J.A.; Tran, T.T.T.; Yang, Q.; Abbott, J.W.; Ayers, S.L.; Young, S.R.; Crarey, E.T.; et al. MRSA and multidrug-resistant Staphylococcus aureus in U.S. retail meats, 2010–2011. Food Microbiol. 2017, 62, 289–297. [Google Scholar] [CrossRef]
  50. Akbar, A.; Anal, A.K. Prevalence and antibiogram study of Salmonella and Staphylococcus aureus in poultry meat. Asian Pac. J. Trop. Biomed. 2013, 3, 163–168. [Google Scholar] [CrossRef] [Green Version]
  51. Mebkhout, F.; Mezali, L.; Hamdi, T.M.; Cantekin, Z.; Ergun, Y.; Ramdani-Bouguessa, N.; Butaye, P. Prevalence and distribution of staphylococcal enterotoxin genes among Staphylococcus aureus isolates from chicken and turkey carcasses in Algeria. J. Hell. Vet. Med. Soc. 2019, 69, 1297–1304. [Google Scholar] [CrossRef] [Green Version]
  52. Govender, V.; Madoroba, E.; Magwedere, K.; Fosgate, G.; Kuonza, L. Prevalence and risk factors contributing to antibiotic-resistant Staphylococcus aureus isolates from poultry meat products in South Africa, 2015–2016. J. S. Afr. Vet. Assoc. 2019, 90, e1–e8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Nworie, A.; Onyema, A.S.; Okekpa, S.I.; Elom, M.O.; Umoh, N.O.; Usanga, V.U.; Ibiam, G.A.; Ukwah, B.N.; Nwadi, L.C.; Ezeruigbo, C.; et al. A Novel Methicillin-Resistant Staphylococcus aureus t11469 and a Poultry Endemic Strain t002 (ST5) Are Present in Chicken in Ebonyi State, Nigeria. Biomed Res. Int. 2017, 2017, 2936461. [Google Scholar] [CrossRef] [Green Version]
  54. Tshipamba, M.E.; Lubanza, N.; Adetunji, M.C.; Mwanza, M. Molecular Characterization and Antibiotic Resistance of Foodborne Pathogens in Street-Vended Ready-to-Eat Meat Sold in South Africa. J. Food Prot. 2018, 81, 1963–1972. [Google Scholar] [CrossRef] [PubMed]
  55. Ou, Q.; Peng, Y.; Lin, D.; Bai, C.; Zhang, T.; Lin, J.; Ye, X.; Yao, Z. A Meta-Analysis of the Global Prevalence Rates of Staphylococcus aureus and Methicillin-Resistant S. aureus Contamination of Different Raw Meat Products. J. Food Prot. 2017, 80, 763–774. [Google Scholar] [CrossRef] [PubMed]
  56. Umeda, K.; Nakamura, H.; Yamamoto, K.; Nishina, N.; Yasufuku, K.; Hirai, Y.; Hirayama, T.; Goto, K.; Hase, A.; Ogasawara, J. Molecular and epidemiological characterization of staphylococcal foodborne outbreak of Staphylococcus aureus harboring seg, sei, sem, sen, seo, and selu genes without production of classical enterotoxins. Int. J. Food Microbiol. 2017, 256, 30–35. [Google Scholar] [CrossRef]
  57. Chessa, D.; Ganau, G.; Mazzarello, V. An overview of Staphylococcus epidermidis and Staphylococcus aureus with a focus on developing countries. J. Infect. Dev. Ctries 2015, 9, 547–550. [Google Scholar] [CrossRef] [PubMed]
  58. Adugna, F.; Pal, M.; Girmay, G. Prevalence and Antibiogram Assessment of Staphylococcus aureus in Beef at Municipal Abattoir and Butcher Shops in Addis Ababa, Ethiopia. Biomed Res. Int. 2018, 2018, 5017685. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  59. Suleiman, A.; Zaria, L.T.; Grema, H.A.; Ahmadu, P. Antimicrobial resistant coagulase positive Staphylococcus aureus from chickens in Maiduguri, Nigeria. Sokoto J. Vet. Sci. 2013, 11, 51–55. [Google Scholar] [CrossRef] [Green Version]
  60. Verhegghe, M.; Crombe, F.; Luyckx, K.; Haesebrouck, F.; Butaye, P.; Herman, L.; Heyndrickx, M.; Rasschaert, G. Prevalence and Genetic Diversity of Livestock-Associated Methicillin-Resistant Staphylococcus aureus on Belgian Pork. J. Food Prot. 2016, 79, 82–89. [Google Scholar] [CrossRef]
  61. Dweba, C.C.; Zishiri, O.T.; El Zowalaty, M.E. Isolation and Molecular Identification of Virulence, Antimicrobial and Heavy Metal Resistance Genes in Livestock-Associated Methicillin-Resistant Staphylococcus aureus. Pathogens 2019, 8, 79. [Google Scholar] [CrossRef] [Green Version]
  62. Khalili, H.; Soltani, R.; Negahban, S.; Abdollahi, A.; Gholami, K. Reliability of disk diffusion test results for the antimicrobial susceptibility testing of nosocomial gram-positive microorganisms: Is E-test method better? Iran. J. Pharm. Res. IJPR 2012, 11, 559. [Google Scholar] [PubMed]
  63. Wu, S.; Huang, J.; Zhang, F.; Wu, Q.; Zhang, J.; Pang, R.; Zeng, H.; Yang, X.; Chen, M.; Wang, J.; et al. Prevalence and characterization of food-related methicillin-resistant Staphylococcus aureus (MRSA) in China. Front. Microbiol. 2019, 10, 304. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Wang, X.; Li, G.; Xia, X.; Yang, B.; Xi, M.; Meng, J. Antimicrobial susceptibility and molecular typing of methicillin-resistant Staphylococcus aureus in retail foods in Shaanxi, China. Foodborne Pathog. Dis. 2014, 11, 281–286. [Google Scholar] [CrossRef] [PubMed]
  65. Papadopoulos, P.; Papadopoulos, T.; Angelidis, A.S.; Boukouvala, E.; Zdragas, A.; Papa, A.; Hadjichristodoulou, C.; Sergelidis, D. Prevalence of Staphylococcus aureus and of methicillin-resistant S. aureus (MRSA) along the production chain of dairy products in north-western Greece. Food Microbiol. 2018, 69, 43–50. [Google Scholar] [CrossRef]
  66. Rajkhowa, S.; Sarma, D.K.; Pegu, S.R. SCCmec typing and antimicrobial resistance of methicillin-resistant Staphylococcus aureus (MRSA) from pigs of Northeast India. Vet. Res. Commun. 2016, 40, 117–122. [Google Scholar] [CrossRef]
  67. Normanno, G.; Dambrosio, A.; Lorusso, V.; Samoilis, G.; Di Taranto, P.; Parisi, A. Methicillin-resistant Staphylococcus aureus (MRSA) in slaughtered pigs and abattoir workers in Italy. Food Microbiol. 2015, 51, 51–56. [Google Scholar] [CrossRef]
  68. Virdis, S.; Scarano, C.; Cossu, F.; Spanu, V.; Spanu, C.; De Santis, E.P. Antibiotic Resistance in Staphylococcus aureus and Coagulase Negative Staphylococci Isolated from Goats with Subclinical Mastitis. Vet. Med. Int. 2010, 2010, 517060. [Google Scholar] [CrossRef] [Green Version]
  69. Richter, A.; Sting, R.; Popp, C.; Rau, J.; Tenhagen, B.A.; Guerra, B.; Hafez, H.M.; Fetsch, A. Prevalence of types of methicillin-resistant Staphylococcus aureus in turkey flocks and personnel attending the animals. Epidemiol. Infect. 2012, 140, 2223–2232. [Google Scholar] [CrossRef] [Green Version]
  70. Founou, L.L.; Founou, R.C.; Allam, M.; Ismail, A.; Finyom Djoko, C.; Essack, S.Y. Genome analysis of methicillin-resistant Staphylococcus aureus isolated from pigs: Detection of the clonal lineage ST398 in Cameroon and South Africa. Zoonoses Public Health 2019, 66, 512–525. [Google Scholar] [CrossRef]
  71. Amoako, D.G.; Somboro, A.M.; Abia, A.L.K.; Allam, M.; Ismail, A.; Bester, L.; Essack, S.Y. Genomic analysis of methicillin-resistant Staphylococcus aureus isolated from poultry and occupational farm workers in Umgungundlovu District, South Africa. Sci. Total Environ. 2019, 670, 704–716. [Google Scholar] [CrossRef]
  72. Mkize, N.; Zishiri, O.T.; Mukaratirwa, S. Genetic characterisation of antimicrobial resistance and virulence genes in Staphylococcus aureus isolated from commercial broiler chickens in the Durban metropolitan area, South Africa. J. S. Afr. Vet. Assoc. 2017, 88, e1–e7. [Google Scholar] [CrossRef] [PubMed]
  73. Karmi, M. Prevalence of methicillin-resistant Staphylococcus aureus in poultry meat in Qena, Egypt. Vet. World 2013, 6, 711–715. [Google Scholar] [CrossRef]
  74. Darwish, W.S.; Atia, A.S.; Reda, L.M.; Elhelaly, A.E.; Thompson, L.A.; Saad Eldin, W.F. Chicken giblets and wastewater samples as possible sources of methicillin-resistant Staphylococcus aureus: Prevalence, enterotoxin production, and antibiotic susceptibility. J. Food Saf. 2018, 38, e12478. [Google Scholar] [CrossRef]
  75. Bakheet, A.; Amen, O.; Habaty, S.; Darwish, S. Prevalence of Staphylococcus aureus In Broiler Chickens with Special Reference to Beta-Lactam Resistance Genes in the Isolated Strains. Alex. J. Vet. Sci. 2018, 59, 25–33. [Google Scholar] [CrossRef]
  76. Momtaz, H.; Dehkordi, F.S.; Rahimi, E.; Asgarifar, A.; Momeni, M. Virulence genes and antimicrobial resistance profiles of Staphylococcus aureus isolated from chicken meat in Isfahan province, Iran. J. Appl. Poult. Res. 2013, 22, 913–921. [Google Scholar] [CrossRef]
  77. Price, L.B.; Stegger, M.; Hasman, H.; Aziz, M.; Larsen, J.; Andersen, P.S.; Pearson, T.; Waters, A.E.; Foster, J.T.; Schupp, J.; et al. Staphylococcus aureus CC398: Host adaptation and emergence of methicillin resistance in livestock. MBio 2012, 3, e00305-11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  78. Uhlemann, A.-C.; Porcella, S.F.; Trivedi, S.; Sullivan, S.B.; Hafer, C.; Kennedy, A.D.; Barbian, K.D.; McCarthy, A.J.; Street, C.; Hirschberg, D.L. Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. MBio 2012, 3, e00027-12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  79. Yuan, W.; Liu, J.; Zhan, Y.; Wang, L.; Jiang, Y.; Zhang, Y.; Sun, N.; Hou, N. Molecular typing revealed the emergence of PVL-positive sequence type 22 methicillin-susceptible Staphylococcus aureus in Urumqi, Northwestern China. Infect. Drug Resist. 2019, 12, 1719. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  80. Cuny, C.; Wieler, L.H.; Witte, W. Livestock-Associated MRSA: The Impact on Humans. Antibiotics 2015, 4, 521–543. [Google Scholar] [CrossRef]
  81. Worthing, K.A.; Abraham, S.; Pang, S.; Coombs, G.W.; Saputra, S.; Jordan, D.; Wong, H.S.; Abraham, R.J.; Trott, D.J.; Norris, J.M. Molecular characterization of methicillin-resistant Staphylococcus aureus isolated from Australian animals and veterinarians. Microb. Drug Resist. 2018, 24, 203–212. [Google Scholar] [CrossRef]
  82. Saei, H.D.; Panahi, M. Genotyping and antimicrobial resistance of Staphylococcus aureus isolates from dairy ruminants: Differences in the distribution of clonal types between cattle and small ruminants. Arch. Microbiol. 2020, 202, 115–125. [Google Scholar] [CrossRef] [PubMed]
  83. Mama, O.M.; Gómez-Sanz, E.; Ruiz-Ripa, L.; Gómez, P.; Torres, C. Diversity of staphylococcal species in food producing animals in Spain, with detection of PVL-positive MRSA ST8 (USA300). Vet. Microbiol. 2019, 233, 5–10. [Google Scholar] [CrossRef] [PubMed]
  84. Strauß, L.; Stegger, M.; Akpaka, P.E.; Alabi, A.; Breurec, S.; Coombs, G.; Egyir, B.; Larsen, A.R.; Laurent, F.; Monecke, S. Origin, evolution, and global transmission of community-acquired Staphylococcus aureus ST8. Proc. Natl. Acad. Sci. USA 2017, 114, E10596–E10604. [Google Scholar] [CrossRef] [Green Version]
  85. Vandenesch, F.; Naimi, T.; Enright, M.C.; Lina, G.; Nimmo, G.R.; Heffernan, H.; Liassine, N.; Bes, M.; Greenland, T.; Reverdy, M.-E. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: Worldwide emergence. Emerg. Infect. Dis. 2003, 9, 978. [Google Scholar] [CrossRef]
  86. Vanderhaeghen, W.; Hermans, K.; Haesebrouck, F.; Butaye, P. Methicillin-resistant Staphylococcus aureus (MRSA) in food production animals. Epidemiol. Infect. 2010, 138, 606–625. [Google Scholar] [CrossRef] [Green Version]
  87. Verhegghe, M.; Pletinckx, L.J.; Crombe, F.; Vandersmissen, T.; Haesebrouck, F.; Butaye, P.; Heyndrickx, M.; Rasschaert, G. Methicillin-resistant Staphylococcus aureus (MRSA) ST398 in pig farms and multispecies farms. Zoonoses Public Health 2013, 60, 366–374. [Google Scholar] [CrossRef]
  88. Crombe, F.; Willems, G.; Dispas, M.; Hallin, M.; Denis, O.; Suetens, C.; Gordts, B.; Struelens, M.; Butaye, P. Prevalence and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus among pigs in Belgium. Microb. Drug Resist. 2012, 18, 125–131. [Google Scholar] [CrossRef] [Green Version]
  89. Beneke, B.; Klees, S.; Stuhrenberg, B.; Fetsch, A.; Kraushaar, B.; Tenhagen, B.A. Prevalence of methicillin-resistant Staphylococcus aureus in a fresh meat pork production chain. J. Food Prot. 2011, 74, 126–129. [Google Scholar] [CrossRef] [PubMed]
  90. Agerso, Y.; Hasman, H.; Cavaco, L.M.; Pedersen, K.; Aarestrup, F.M. Study of methicillin resistant Staphylococcus aureus (MRSA) in Danish pigs at slaughter and in imported retail meat reveals a novel MRSA type in slaughter pigs. Vet. Microbiol. 2012, 157, 246–250. [Google Scholar]
  91. Boost, M.V.; Wong, A.; Ho, J.; O’Donoghue, M. Isolation of Methicillin-Resistant Staphylococcus aureus (MRSA) from Retail Meats in Hong Kong. Foodborne Pathog. Dis. 2013, 10, 705–710. [Google Scholar] [CrossRef] [PubMed]
  92. Tanih, N.F.; Sekwadi, E.; Ndip, R.N.; Bessong, P.O. Detection of pathogenic Escherichia coli and Staphylococcus aureus from cattle and pigs slaughtered in abattoirs in Vhembe District, South Africa. Sci. World J. 2015, 2015, 195972. [Google Scholar] [CrossRef] [Green Version]
  93. Okunlola, I.; Ayandele, A. Prevalence and antimicrobial susceptibility of Methicillin-resistant Staphylococcus aureus (MRSA) among pigs in selected farms in Ilora, South Western Nigeria. Eur. J. Exp. Biol. 2015, 5, 50–56. [Google Scholar]
  94. Kreausukon, K.; Fetsch, A.; Kraushaar, B.; Alt, K.; Muller, K.; Kromker, V.; Zessin, K.H.; Kasbohrer, A.; Tenhagen, B.A. Prevalence, antimicrobial resistance, and molecular characterization of methicillin-resistant Staphylococcus aureus from bulk tank milk of dairy herds. J. Dairy Sci. 2012, 95, 4382–4388. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  95. Huber, H.; Giezendanner, N.; Stephan, R.; Zweifel, C. Genotypes, antibiotic resistance profiles and microarray-based characterization of methicillin-resistant Staphylococcus aureus strains isolated from livestock and veterinarians in Switzerland. Zoonoses Public Health 2011, 58, 343–349. [Google Scholar] [CrossRef] [PubMed]
  96. Huys, G.; D’Haene, K.; Van Eldere, J.; von Holy, A.; Swings, J. Molecular diversity and characterization of tetracycline-resistant Staphylococcus aureus isolates from a poultry processing plant. Appl Environ. Microbiol. 2005, 71, 574–579. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  97. Gómez-Sanz, E.; Torres, C.; Lozano, C.; Fernández-Pérez, R.; Aspiroz, C.; Ruiz-Larrea, F.; Zarazaga, M. Detection, Molecular Characterization, and Clonal Diversity of Methicillin-Resistant Staphylococcus aureus CC398 and CC97 in Spanish Slaughter Pigs of Different Age Groups. Foodborne Pathog. Dis. 2010, 7, 1269–1277. [Google Scholar] [CrossRef]
  98. Satola, S.W.; Farley, M.M.; Anderson, K.F.; Patel, J.B. Comparison of detection methods for heteroresistant vancomycin-intermediate Staphylococcus aureus, with the population analysis profile method as the reference method. J. Clin. Microbiol. 2011, 49, 177–183. [Google Scholar] [CrossRef] [Green Version]
  99. Srinivasan, A.; Dick, J.D.; Perl, T.M. Vancomycin resistance in staphylococci. Clin. Microbiol. Rev. 2002, 15, 430–438. [Google Scholar] [CrossRef] [Green Version]
  100. Ahmed, W.A.; Hotzel, H.; Neubauer, H.; El-tawab, A.A.A.; Tomaso, H.; Sobhy, M.M.; El Hofy, F.I. Antimicrobial Resistance Genes Associated with Enterococci from Poultry in Egypt, First Reporting of mecA in Enterococcus from Poultry Source. Adv. Anim. Vet. Sci. 2020, 8, 570–581. [Google Scholar] [CrossRef]
  101. Mahros, M.M.; Abd-Elghany, S.M.; Sallam, K.I. Multidrug-, methicillin-, and vancomycin-resistant Staphylococcus aureus isolated from ready-to-eat meat sandwiches: An ongoing food and public health concern. Int. J. food Microbiol. 2021, 346, 109165. [Google Scholar] [CrossRef]
  102. El-Zamkan, M.A.; Mubarak, A.G.; Ali, A.O. Prevalence and phylogenetic relationship among methicillin-and vancomycin-resistant Staphylococci isolated from hospital’s dairy food, food handlers, and patients. J. Adv. Vet. Anim. Res. 2019, 6, 463. [Google Scholar] [CrossRef] [PubMed]
  103. Taha, A.E.; Badr, M.F.; El-Morsy, F.E.; Hammad, E. Report of β-lactam antibiotic-induced vancomycin-resistant Staphylococcus aureus from a university hospital in Egypt. New Microbes New Infect. 2019, 29, 100507. [Google Scholar] [CrossRef] [PubMed]
  104. Van Rensburg, M.J.; Madikane, V.E.; Whitelaw, A.; Chachage, M.; Haffejee, S.; Elisha, B.G. The dominant methicillin-resistant Staphylococcus aureus clone from hospitals in Cape Town has an unusual genotype: ST612. Clin. Microbiol. Infect. 2011, 17, 785–792. [Google Scholar] [CrossRef] [Green Version]
  105. Axon, J.; Carrick, J.; Barton, M.; Collins, N.; Russell, C.; Kiehne, J.; Coombs, G. Methicillin-resistant Staphylococcus aureus in a population of horses in Australia. Aust. Vet. J. 2011, 89, 221–225. [Google Scholar] [CrossRef]
  106. Sato, T.; Usui, M.; Konishi, N.; Kai, A.; Matsui, H.; Hanaki, H.; Tamura, Y. Closely related methicillin-resistant Staphylococcus aureus isolates from retail meat, cows with mastitis, and humans in Japan. PLoS ONE 2017, 12, e0187319. [Google Scholar] [CrossRef]
  107. Murphy, R.J.; Ramsay, J.P.; Lee, Y.T.; Pang, S.; O’Dea, M.A.; Pearson, J.C.; Axon, J.E.; Raby, E.; Abdulgader, S.M.; Whitelaw, A. Multiple introductions of methicillin-resistant Staphylococcus aureus ST612 into Western Australia associated both with human and equine reservoirs. Int. J. Antimicrob. Agents 2019, 54, 681–685. [Google Scholar] [CrossRef]
  108. Groves, M.D.; Crouch, B.; Coombs, G.W.; Jordan, D.; Pang, S.; Barton, M.D.; Giffard, P.; Abraham, S.; Trott, D.J. Molecular epidemiology of methicillin-resistant Staphylococcus aureus isolated from Australian veterinarians. PLoS ONE 2016, 11, e0146034. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  109. Amoako, D.G.; Somboro, A.M.; Abia, A.L.K.; Allam, M.; Ismail, A.; Bester, L.A.; Essack, S.Y. Genome mining and comparative pathogenomic analysis of an endemic methicillin-resistant Staphylococcus aureus (MRSA) clone, ST612-CC8-t1257-SCCmec_IVd (2B), isolated in South Africa. Pathogens 2019, 8, 166. [Google Scholar] [CrossRef] [Green Version]
  110. Amoako, D.G.; Somboro, A.M.; Abia, A.L.K.; Allam, M.; Ismail, A.; Bester, L.A.; Essack, S.Y. Whole-Genome Shotgun Sequence of Drug-Resistant Staphylococcus aureus Strain SA9, Isolated from a Slaughterhouse Chicken Carcass in South Africa. Microbiol. Resour. Announc. 2019, 8, e00489-19. [Google Scholar] [CrossRef] [Green Version]
  111. Peeters, L.E.; Argudín, M.A.; Azadikhah, S.; Butaye, P. Antimicrobial resistance and population structure of Staphylococcus aureus recovered from pigs farms. Vet. Microbiol. 2015, 180, 151–156. [Google Scholar] [CrossRef]
  112. Nemeghaire, S.; Roelandt, S.; Argudín, M.A.; Haesebrouck, F.; Butaye, P. Characterization of methicillin-resistant Staphylococcus aureus from healthy carrier chickens. Avian Pathol. 2013, 42, 342–346. [Google Scholar] [CrossRef] [PubMed]
  113. Nemeghaire, S.; Argudín, M.A.; Haesebrouck, F.; Butaye, P. Epidemiology and molecular characterization of methicillin-resistant Staphylococcus aureus nasal carriage isolates from bovines. BMC Vet. Res. 2014, 10, 153. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  114. Schaumburg, F.; Alabi, A.S.; Frielinghaus, L.; Grobusch, M.P.; Kock, R.; Becker, K.; Issifou, S.; Kremsner, P.G.; Peters, G.; Mellmann, A. The risk to import ESBL-producing Enterobacteriaceae and Staphylococcus aureus through chicken meat trade in Gabon. BMC Microbiol. 2014, 14, 286. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  115. Shang, W.; Hu, Q.; Yuan, W.; Cheng, H.; Yang, J.; Hu, Z.; Yuan, J.; Zhang, X.; Peng, H.; Yang, Y. Comparative fitness and determinants for the characteristic drug resistance of ST239-MRSA-III-t030 and ST239-MRSA-III-t037 strains isolated in China. Microb. Drug Resist. 2016, 22, 185–192. [Google Scholar] [CrossRef] [PubMed]
  116. Oosthuysen, W.; Orth, H.; Lombard, C.; Sinha, B.; Wasserman, E. Population structure analyses of Staphylococcus aureus at Tygerberg Hospital, South Africa, reveals a diverse population, a high prevalence of Panton–Valentine leukocidin genes, and unique local methicillin-resistant S. aureus clones. Clin. Microbiol. Infect. 2014, 20, 652–659. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  117. Abdulgader, S.M.; Shittu, A.O.; Nicol, M.P.; Kaba, M. Molecular epidemiology of Methicillin-resistant Staphylococcus aureus in Africa: A systematic review. Front. Microbiol. 2015, 6, 348. [Google Scholar] [CrossRef] [PubMed]
Table
Table 1. Prevalence of S. aureus (non-MRSA) in raw unprocessed red meat in African countries.
Table 1. Prevalence of S. aureus (non-MRSA) in raw unprocessed red meat in African countries.
Meat TypeYearCountryNo. of Tested SamplesNo. of S. aureus positivePercentage Prevalence (CI) *Reference
Beef2010Ivory coast801215 (8–25)[24]
2018South Africa1884825 (19.5–32)[25]
2015–2016South Africa50010120 (16.8–24)[26]
2009Nigeria752128 (18.2–40)[27]
2009–2014Algeria46525555 (50.2–59)[28]
2015Egypt27933 (16.5–54)[29]
2018Egypt25416 (4.5–36)[30]
Total 136045033.08 (30.6–36)
Pork2009Nigeria75912 (5.6–22)[27]
2018South Africa200147 (3.9–11)[26]
2018South Africa36822 (10.1–39)[25]
2010Ivory Coast8056.25 (2.1–14)[24]
2015Canary island 3005819 (15–24)[31]
Total 6919413.6 (11.1–16)
Goat meat2009Nigeria75912 (5.6–22)[27]
Camel meat2017Egypt2002914.5 (9.9–20)[32]
Sheep/lamb South Africa300103.3 (1.6–6)[26]
South Africa864653.48 (42.4–64)[25]
Total 3865614.5 (11.1–18)
Unspecified raw red meat Nigeria15339.15 (0.4–6)[33]
Nigeria605898.33 (88.5–100)[34]
Total 2136128.6 (22.7–35)
Overall total285369924.5 (22.9–26)
* Confidence interval: the confidence interval (CI) was set at 95% and calculated based on the exact binomial method [35].
Table
Table 2. Prevalence of S. aureus in raw unprocessed poultry in African countries.
Table 2. Prevalence of S. aureus in raw unprocessed poultry in African countries.
Meat TypeYearCountryNo. Tested SamplesNo. S. aureus PositivePrevalence % (CI)Reference
Turkey2012–2013Algeria703245 (33.7–58)[51]
Chicken2009Nigeria756080 (69.2–88)[27]
2010–2011Tunisia844151.19 (37.7–60)[47]
2009–2014Algeria8375156718.71 (17.9–20)[28]
2015Egypt5036 (1.3–17)[29]
2015–2016South Africa31110634.1 (28.8–40)[52]
2017Nigeria180023213 (11.4–15)[53]
2012–2013Algeria31512840.63 (35.2–46)[51]
Total11,111213919 (18.5–20)
Total Overall11,080216919.6 (18.8–20)
Table
Table 3. Prevalence of S. aureus in raw processed meat.
Table 3. Prevalence of S. aureus in raw processed meat.
Meat TypeYearCountryNo. Tested SamplesNo. S. aureus PositivePrevalence % (CI)Reference
Beef2013Nigeria1471510,2 (5.8–16)[33]
2018Egypt1001620 (9.4–25)[30]
Total2473113 (8.7–17)
Table
Table 4. Prevalence of S. aureus in ready-to-eat meat.
Table 4. Prevalence of S. aureus in ready-to-eat meat.
Meat TypeYearCountryNo. Tested SamplesNo. S. aureus PositivePrevalence % (CI)Reference
Chicken2015–2016South Africa453.758.3 (2.5–21)[54]
Table
Table 5. Characteristics of antimicrobial resistance of S. aureus from meat and meat products in African countries.
Table 5. Characteristics of antimicrobial resistance of S. aureus from meat and meat products in African countries.
Antimicrobial ClassesAntimicrobial AgentsNumber Tested Number ResistantPercentage % (CI)
Penicillins
Amino-penicillins
Penicillin-resistant penicillin		Penicillin G198136318 (16.5–20)
Ampicillin22911450 (43.1–56)
Oxacillin207125914 (11.1–14)
CephalosporinsCeftaroline1262923 (15.7–33)
Cefoxitin19191649 (7.3–10)
GlycopeptidesVancomycin1951140.7 (0.4–1)
AminoglycosidesGentamicin2085201 (0.1–1)
Amikacin961919.79 (12.4–29)
Kanamycin1881975 (4.2–6)
MacrolidesErythromycin204922210.8 (9.5–12)
TetracyclinesTetracycline18651236.5 (5.5–8)
Doxycycline1363727 (19.9–37)
Minocycline1011211 (6.3–20)
FluoroquinolonesCiprofloxacin24872.8 (1.1–6)
Ofloxacin543157 (43.2–71)
LincosamidesClindamycin1896433.8 (27.2–64)
Folate pathway inhibitorsTrimethoprim/sulphonamides1949512.6 (2–3)
PhenicolsChloramphenicol14253.5 (0.9–6)
OxazolidinonesLinezolid10298.8 (4.1–16)
References: [25,26,27,28,29,30,32,33,47,52,54,59,70,71,72,73,74,75].
Table
Table 6. Antimicrobial resistance genes in S. aureus from different meat products in African countries.
Table 6. Antimicrobial resistance genes in S. aureus from different meat products in African countries.
CountryMeat TypeType of Strain (Number Tested)Resistance Genes DetectedReference
TunisiaChickenMSSA (22)erm(A), erm(C), tet(M), tet(K), erm(T), tet(L), aph (3′)-IIIa, ant (4′), msrA[47]
South AfricaBeef, sheep, porkMSSA (98)blaZ, tet(K), tet(M), msrA, ant (4′)-la, aph (3′)-1-IIIa[26]
Table
Table 7. Sequence type of meat isolates from Tunisia.
Table 7. Sequence type of meat isolates from Tunisia.
SpeciesType of Strain (Number)Spa TypeSequence Type (ST)Origin of the SampleReference
ChickenMSSA (2)t899ST 398Poultry market meat[47]
ChickenMSSA (1)t13938ST 398Supermarket meat[47]
VealMSSA (1)t034ST 398Butchery meat[47]
ChickenMSSA (1)t005ST 22Poultry market meat[47]
SheepMSSA (1)t008ST 8Butchery meat[47]
Table
Table 8. Prevalence of methicillin-resistant S. aureus (MRSA) in different types of meat from Africa.
Table 8. Prevalence of methicillin-resistant S. aureus (MRSA) in different types of meat from Africa.
Meat TypeYearCountryStudied SamplesMRSA PositiveMRSA Detection MethodPrevalence % (CI)Reference
Raw beef meat2015SA17630PCR 117 (11.8–23)[92]
2016Nigeria4010PCR25 (12.7–41)[46]
2016SA & Cameron1445WGS 23.47 (1.1–8)[70]
2018Egypt1004PCR4 (1.1–10)[30]
2018SA5001PCR0.2 (0–1)[26]
Total 81650 6.12 (4.6–8)
Raw pork meat2015Nigeria20018Oxacillin disc-Kirby Bauer disk diffusion9 (5.4–14)[93]
2015SA17620PCR11.36 (7.1–17)[92]
2016Nigeria5614PCR25 (14.4–38)[46]
Total 43252 12 (9.1–15)
Raw poultry2010–2011Tunesia432PCR4.65 (0.6–16)[47]
2013Egypt5024Latex-slide agglutination48 (33.7–63)[73]
2016Nigeria306PCR20 (7.7–39)[46]
2017SA19492PCR47 (40.2–55)[72]
2017Nigeria180015PCR0.8 (0.5–1)[53]
2018Egypt8112PCR14.8 (7.9–24)[75]
2018Egypt808PCR10 (4.4–19)[71,74]
2019SA1455Real-time PCR3.4 (1.1–8)[71]
Total 2423164 6.76 (5.8–8)
Processed poultry2013Egypt7527Latex-slide agglutination36 (25.2–48)[73]
Total 3746293 7.8 (7–9)
1 Polymerase chain reaction; 2 Whole-genome sequencing.
Table
Table 9. Characteristics of antimicrobial resistance of methicillin-resistant S. aureus (MRSA) from meat and meat products in African countries.
Table 9. Characteristics of antimicrobial resistance of methicillin-resistant S. aureus (MRSA) from meat and meat products in African countries.
Antimicrobial ClassesAntimicrobial AgentsNumber of TestedNumber of ResistantPercentage % (CI)
Penicillins Amino-penicillins Penicillin-resistant penicillinPenicillin G494693 (83.1–99)
Ampicillin1278163 (54.8–72)
Amoxicillin524790 (79–97)
Oxacillin807695 (87.7–99)
Methicillin2828100 (87.7–100)
Flucloxacillin181689 (65.3–99)
CephalosporinsCephalexin181794 (72.7–100)
Cefoxitin1319975 (67.3–83)
Cefotaxime44100 (39.8–100)
Cefuroxime151386 (59.5–98)
GlycopeptidesVancomycin922527 (18.4–37)
AminoglycosidesGentamicin1145447 (37.9–57)
Amikacin6350 (11.8–88)
Kanamycin161168 (41.3–88)
Streptomycin963031 (22.2–42)
MacrolidesErythromycin1509462 (54.4–70)
TetracyclinesTetracycline13412391 (85.8–96)
Doxycycline161168 (41.3–89)
Oxytetracycline625080 (68.6–90)
FluoroquinolonesCiprofloxacin171482 (56.6–96)
Enrofloxacin12758 (27.7–85)
Nalidixic acid545296 (87.3–100)
LincosamidesClindamycin393795 (82.7–99)
Folate pathway inhibitorsTrimethoprim/sulphonamides 1466343 (35–52)
PhenicolsChloramphenicol352571 (53.7–85)
References: [26,30,46,47,53,70,71,72,73,74,75,92,93].
Table
Table 10. Antimicrobial resistance genes of MRSA from African countries.
Table 10. Antimicrobial resistance genes of MRSA from African countries.
CountryMeat TypeTyped Strain (Number Tested)Resistance Genes DetectedReference
South AfricaBeefMRSA (1)mecA[26]
NigeriaBeef, chicken, porkMRSA (49)mecA[46]
TunisiaChickenMRSA (2)mecA, ermC, tetM[47]
South AfricaChicken carcassMRSA (2)mecA, blaZ, aac(6′)-aph(″), erm(C), mph[71]
EgyptCamel carcassMR (25)-VRSA (14)mecA, vanA, vanB[32]
EgyptBeef meatMRSA (4)mecA, tetK, vanA[30]
South AfricaBroiler chickenMRSA (73)mecA, blaZ, tetK[72]
Table
Table 11. Sequence tMype and spa type of different meat isolates from two African countries.
Table 11. Sequence tMype and spa type of different meat isolates from two African countries.
SpeciesType of Strain (Number)Spa TypeSequence Type (ST)Origin of the SampleReference
ChickenMRSAt102ST30Farm[47]
ChickenMRSAt4358ST398Poultry market[47]
CarcassMRSAt1257ST612Retail point[71]
ChickenMRSAt037ST239Slaughterhouse [110]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Thwala, T.; Madoroba, E.; Basson, A.; Butaye, P. Prevalence and Characteristics of Staphylococcus aureus Associated with Meat and Meat Products in African Countries: A Review. Antibiotics 2021, 10, 1108. https://doi.org/10.3390/antibiotics10091108

AMA Style

Thwala T, Madoroba E, Basson A, Butaye P. Prevalence and Characteristics of Staphylococcus aureus Associated with Meat and Meat Products in African Countries: A Review. Antibiotics. 2021; 10(9):1108. https://doi.org/10.3390/antibiotics10091108

Chicago/Turabian Style

Thwala, Thembeka, Evelyn Madoroba, Albert Basson, and Patrick Butaye. 2021. "Prevalence and Characteristics of Staphylococcus aureus Associated with Meat and Meat Products in African Countries: A Review" Antibiotics 10, no. 9: 1108. https://doi.org/10.3390/antibiotics10091108

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop