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Article

Microbiological Quality and Safety of Fresh Pork Meat with Special Reference to Methicillin-Resistant S. aureus and Other Staphylococci

by
Alba Martinez-Laorden
,
Celia Arraiz-Fernandez
,
Gonzalo Ibañez-Torija
and
Elena Gonzalez-Fandos
*
Food Technology Department, CIVA Research Center, University of La Rioja, Madre de Dios 53, 26006 Logrono, La Rioja, Spain
*
Author to whom correspondence should be addressed.
Vet. Sci. 2025, 12(6), 568; https://doi.org/10.3390/vetsci12060568
Submission received: 2 May 2025 / Revised: 2 June 2025 / Accepted: 3 June 2025 / Published: 10 June 2025
Versions Notes

Simple Summary

Nowadays, there is a great concern about S. aureus resistant to methicillin (MRSA). This pathogen poses a major challenge to both human and animal health due to the severity of the infections that they can cause. MRSA can be present in pork meat, being the primary reservoir of the porcine nasopharyngeal tract, although cross-contamination during processing can also occur. This study evaluates the presence of this pathogen in pork meat as well as its antimicrobial resistance. The results show that multi-resistant MRSA can be present in meat. Thus, additional measures should be taken to control this pathogen in pork meat.

Abstract

Nowadays, there is a great concern about the prevalence of multidrug-resistant bacteria in meat, especially Staphylococcus aureus resistant to methicillin (MRSA). The aim of this work was to evaluate the microbiological quality of fresh pork meat and the presence and resistance of S. aureus and other Staphylococcus spp., Mammaliicoccus spp., and Macrococcus spp. to methicillin and other antibiotics. A total of 39 fresh pork meat samples were analyzed. MRSA was isolated from one sample, being resistant to eight antimicrobial families, including aminoglycosides, β-lactams, lincosamides, macrolides, sulfonamides, tetracycline, and others such as fusidic acid, and mupirocin. Also, other multidrug-resistant strains with resistance to 5 or 6 antimicrobial families were isolated including Staphylococcus succinus, Mammaliicoccus sciuri, and Macrococcus caseolyticus. Additional measures should be taken to control MRSA in pork meat.

1. Introduction

Pork meat contains a large amount of nutrients that are essential for human development and for preventing deficiencies, making it a key component of the diet [1,2,3]. It is the most widely consumed meat, with annual consumption exceeding 115 million tons, and it is expected to grow by 8% in 2033 [4]. In the European Union, and especially in Spain, the pork sector plays an important role both in terms of production volume and economic value, with Spain being the largest producer of pork in the EU [5].
Fresh meat is a highly perishable food and is susceptible to microbiological contamination [6]. This contamination can occur at various stages of the production chain, from slaughter to retail sale [7]. Microorganisms identified in pork meat and pigs include Yersinia enterocolitica, Escherichia coli, S. aureus, Enterococcus spp., Listeria monocytogenes, Campylobacter spp., Clostridium spp., Salmonella spp., and Pseudomonas spp. [8,9,10,11,12,13,14,15,16,17,18,19,20]. Some of these microorganisms are spoilage organisms, while others are pathogenic. The latter can cause infections in animals and humans and represent a public health risk, particularly when they exhibit resistance to commonly used antibiotic treatments [21,22].
Among the most concerning pathogens in pork meat is S. aureus. S. aureus and other staphylococci are associated with cross-contamination of pork, with the primary reservoir being the porcine nasopharyngeal tract. Therefore, most contamination events are attributed to the slaughter and carcass-cutting processes [23]. Several studies have reported the presence of S. aureus in a wide range of pork meat samples, with prevalence rates ranging from 6% to 100% [9,10,24,25]. A particularly alarming aspect of this pathogen is its resistance to methicillin, which gives rise to methicillin-resistant S. aureus (MRSA). These strains pose a major challenge to both human and animal health due to the severity of the infections they can cause, as they produce toxins and enterotoxins capable of inducing food poisoning, as well as urinary, respiratory, and bloodstream infections [25,26,27]. Pigs have been identified as a significant reservoir of MRSA, highlighting the urgent need to implement control measures during the production and processing stages [28]. Similarly, the presence of MRSA strains has been detected in pork meat [10,24,25,29,30,31,32,33]. Likewise, the presence of other methicillin-resistant staphylococci (MRS) has also been reported in pigs [34].
Due to the use of antibiotics in livestock, animals have become one of the main reservoirs of antibiotic-resistant bacteria, such as Staphylococcus spp., which can spread to humans through the consumption of contaminated meat, among other routes [35,36]. This poses a significant risk to both human and animal health, as it considerably reduces the effectiveness of antibiotic treatments [37]. In response to this issue, the World Health Organization (WHO), the Food and Agriculture Organization of the United Nations (FAO), and the World Organisation for Animal Health (OIE) promote the “One Health” concept, which advocates for a unified approach to human, animal, and environmental health, with the aim of generating rapid and effective responses to emerging health challenges [38,39].
The microbiological analysis of pork available on the market is essential not only for detecting potential microbiological risks but also for evaluating the effectiveness of hygiene and preservation practices at retail points. In Spain, although strict food safety regulations are in place, microbiological surveillance at the retail level remains a critical point for the prevention of foodborne illnesses [40].
The objective of this study is to characterize the microbiological profile of fresh pork meat, as well as the resistance of S. aureus and other Staphylococcus spp., Mammaliicoccus spp., and Macrococcus spp. to methicillin and other antibiotics.

2. Materials and Methods

2.1. Sampling and Microbiological Evaluation

A total of 39 fresh pork meat samples were obtained from 9 different retail locations in La Rioja, Spain. The samples were collected between January 2020 and January 2021 as part of a preliminary study focused on detecting antibiotics in meat [41]. The number of samples was determined based on consumption data, product availability, and the variety of commercial brands [42]. The samples were ensured to meet optimal storage standards, maintaining a temperature of 4 °C from the time of purchase until arrival at the laboratory. For microbiological analyses, 10 g of pork meat was homogenized using a stomacher (IUL Instruments, Barcelona, Spain) and sterile peptone water (0.1% w/v) (Oxoid, Basingstoke, Hampshire, UK). The following determinations were carried out: Enterobacteriaceae (Oxoid), Pseudomonas spp. (Scharlau, Barcelona, Spain), mesophilic bacteria (Scharlau), and staphylococci (Oxoid), as well as the detection of methicillin-resistant S. aureus using ChromID MRSA medium (Biomerieux, Marcy l’Etoile, France), as previously described by Martínez-Laorden et al. [43,44].

2.2. Isolation and Identification of Strains

Five colonies per medium and sample were selected for strain isolation and identification. The selected colonies were purified using brain–heart infusion broth (Scharlau) and tryptic soy agar (Scharlau) and were then stored at −80 °C. Identification of the purified isolates was performed using MALDI-TOF mass spectrometry (Bruker, Daltonik, Bremen, Germany).

2.3. Phenotypic Confirmation of Methicillin-Resistant Micrococcaceae

Phenotypic determination of methicillin-resistant Staphylococcus spp., Mammaliicoccus spp., and Macrococcus spp. was conducted following the guidelines of the Clinical Laboratory Standards Institute using the disc diffusion technique [45]. A strain of S. aureus sensitive to methicillin and another resistant to methicillin belonging to the collection of the University of La Rioja were included for quality control.

2.4. Phenotypic Evaluation Assay of Staphylococcus spp., Mammaliicoccus spp., and Macrococcus caseolyticus

A phenotypic resistance evaluation assay was performed on Staphylococcus spp., Mammaliicoccus spp., and Macrococcus caseolyticus strains following the disc diffusion method as described by Martínez-Laorden et al. [43,44]. The following antibiotics were used: vancomycin, lincomycin, levofloxacin, gentamicin, ceftaroline, nitrofurantoin, ciprofloxacin, fusidic acid, tedizolid, amikacin, enrofloxacin, kanamycin, linezolid, minocycline, gatifloxacin, erythromycin, ampicillin, chloramphenicol, mupirocin, quinupristin/dalfopristin, trimethoprim, benzylpenicillin, streptomycin, rifampicin, norfloxacin, sulfadiazine, cefoxitin, trimethoprim-sulfamethoxazole, clindamycin, tobramycin, penicillin, doxycycline, tetracycline, and tylosin (Oxoid). A strain was considered multiresistant when it showed resistance to three or more families of antibiotics [43,44].

2.5. Statistical Analysis

Statistical analysis was carried out using SPSS software version 28.0.1.1 (IBM SPSS Statistics, Armonk, NY, USA). Tukey’s test for comparison of means was performed using the same program. The level of significance was determined at p < 0.05.

3. Results

Table 1 shows the microbiological counts obtained from fresh pork meat samples. Mesophilic bacteria showed the highest values, being detected in all samples (mean: 4.93 ± 1.37 log CFU/g). Pseudomonas spp. was found in 50% of the samples, with a mean of 3.89 ± 1.17 log CFU/g, while Enterobacteriaceae showed a mean of 3.46 ± 0.86 log CFU/g, with 35.9% of the samples exceeding 1 log CFU/g. Finally, staphylococci showed the lowest counts (mean: 2.16 ± 0.74 log CFU/g), although they were present in a considerable number of samples.
A total of 113 strains were isolated from the PCA medium, distributed across various microbial groups as shown in Table 2. The predominant species was Brochothrix thermosphacta (26.55%), followed by the genus Pseudomonas spp. (22.12%), with Pseudomnas fragi (12.39%) and Pseudomonas lundensis (7.96%) being the most frequently identified. Within the lactic acid bacteria (LAB) (19.47%), Carnobacterium divergens (14.16%) and Carnobacterium maltaromaticum (2.65%) were the most notable. The Micrococcaceae represented 12.39% of the total. Enterobacteriaceae made up 8.85% of the isolates, with Rahnella insidiosa (3.54%) and Hafnia alvei (2.65%) being the most predominant.
Regarding the Pseudomonas genus isolated from the specific agar for this group, a total of 13 different species were identified as can be seen in Table 3. The most prevalent was Pseudomonas libanensis, with 32 isolates, representing 41.03% of the total, followed by Pseudomonas fluorescens (14.10%) and Pseudomonas azotoformans (10.26%). Other species with notable presence included P. antarctica (8.97%) and Pseudomonas extremorientalis (6.41%). Less common species, such as Pseudomonas poae, Pseudomonas rhodesiae, Pseudomonas. tolaasii, and Pseudomonas trivialis, were represented by a single isolate each (1.28%).
Regarding the species identified within the Enterobacteriaceae group and other Gram-negative fermentative bacilli isolated from agar MacConkey, shown in Table 3, 12 different species were observed, with Serratia liquefaciens being the most prevalent (32.31%), followed by Rahnella aquatilis (20%) and Hafnia alvei (13.85%). Also, Ewingella americana (7.69%), Buttiaxella warmboldiae (7.69%), Klebsiella oxytoca (4.62%), Pantoea agglomerans, (4.62%), and Buttiaxella gaviniae (4.62%) were isolated from fresh pork meat. The detection of Yersinia enterocolitica is noteworthy, although it occurred at a low frequency (1.54%), due to its relevance as a foodborne pathogen.
Regarding the Gram-positive cocci isolated from mannitol salt agar presented in Table 3, 10 different species were identified, with Staphylococcus saprophyticus predominating (38.78%), followed by Staphylococcus warneri (12.24%), and Macrococcus caseolyticus (12.24%). Other species from the Staphylococcus spp. were also detected, such as Staphylococcus equorum (10.20%), Staphylococcus epidermidis (4.08%), and Staphylococcus succinus (4.08%), in addition to members of the Mammaliicoccus spp., such as Mammaliicoccus sciuri (8.16%), Mammaliicoccus vitulinus (6.12%), and Mammaliicoccus fleurettii (2.04%).
With the use of ChromID MRSA medium, MRSA was detected in only one sample, and confirmed as S. aureus by MALDI-TOF.
Table 4 presents the antimicrobial resistance phenotypic profile of various Staphylococcus spp., Mammaliicoccus spp., and Macrococcus caseolyticus strains isolated from fresh pork meat. The presence of multidrug resistance in several strains is highlighted, defined as resistance to three or more classes of antibiotics. In particular, S. aureus isolated from ChromID MRSA medium showed resistance to eight antimicrobial families, including aminoglycosides (amikacin, streptomycin, tobramycin), β-lactams (cefoxitin), lincosamides (clindamycin), macrolides (lincomycin), sulfonamides (sulfadiazine), tetracyclines (tetracycline), and others such as fusidic acid and mupirocin. This strain was also classified as methicillin-resistant (MR).
Other multidrug-resistant strains included S. succinus, M. sciuri, and Macrococcus caseolyticus, showing resistance to 5 or 6 antimicrobial families and also classified as methicillin-resistant.

4. Discussion

Several studies have established that mesophilic levels ranging from 6 to 8 log CFU/g are associated with pork in good quality condition, while values exceeding these indicate deteriorating and poor meat quality [46,47]. Based on this parameter, the current study detected a mesophilic mean count of 4.93 ± 1.37 log CFU/g, indicating an appropriate quality state of the analyzed pork according to the mentioned criteria. These results are higher than those found by Yan et al. [48], who described counts of 2.33 ± 0.02 log CFU/g in pork samples purchased in China.
Other authors report mesophilic counts in pork ranging from 2.92 to 5.34 log CFU/g, data like those obtained in our study and positively correlating with the quality criteria mentioned earlier [49,50,51]. In addition, the observed differences may be due to differences in storage conditions and storage time of the samples [52].
In our current study, B. thermosphacta and Pseudomonas spp. were identified as the predominant group in the microbiota of the analyzed samples. They were followed by lactic acid bacteria (LAB), Micrococcaceae, Enterobacteriaceae, other Gram-negative bacteria (Acinetobacter spp., Moraxella osloensis, and Stenotrophomonas rhizophila), and other Gram-positive bacteria (Dermacoccus nishinomiyaensis). Pseudomonas spp. and B. thermosphacta have been previously described as the main bacterial agents responsible for meat spoilage, including pork meat [43,44,53]. These findings correspond with those mentioned by other authors, such as Papadopoulou et al. [54], who pointed out Pseudomonas spp., B. thermosphacta, LAB, and Enterobacteriaceae as the main bacterial groups detected in pork meat samples in Greece. It is noteworthy that elevated levels of B. thermosphacta could be associated with an unacceptable quality state pork meat, as this bacterium is linked to food spoilage [55].
In relation to Pseudomonas spp. counts, in this study, mean values of 3.89 ± 1.17 log CFU/g were observed. Similar values, but somewhat higher have been reported by other authors, who observed Pseudomonas spp. counts in pork between 2.99 and 3.56 log CFU/g [56,57].
In this study, the presence of Pseudomonas spp. was observed, with isolates identified as P. libanensis, P. fluorescens, P. azotoformans, P. antarctica, P. veronii, P. fragi, P. synxantha, P. marginalis, P. rhodesiae, P. tolaasii, P. poae, P. lundensis, P. extremorientalis, and P. trivialis. The presence of Pseudomonas spp. is associated with food contamination [58,59]. Additionally, other authors have reported the presence of P. fragi, P. libanensis, P. synxantha, P. poae, P. trivialis, P. tolaasii, and P. fluorescens, among others, isolated from pork samples in Italy [60], as well as the species P. aeruginosa, P. brenneri, P. cedrina, P. fulva, P. gesardii, P. kilonensis, P. orientalis, P. proteolytica, P. putida, and P. taetrolens, which were not identified in the present investigation. Authors such as Dorn-In et al. [61] also identified several species of Pseudomonas spp. in samples of fresh pork meat purchased in Germany.
The Food and Agriculture Organization (FAO) considers, as a meat quality criterion for consumption, that it is suitable if Enterobacteriaceae counts are below 3 log CFU/g [62]. The mean of the counts in the present study exceeds this value, 3.46 ± 0.86 log CFU/g, which could indicate the presence of the beginning of meat spoilage. Other studies have reported Enterobacteriaceae counts in pork ranging from 1 to 2.61 log CFU/g, values that would meet the mentioned quality criteria [49,50]. In China, Liang et al. [57] observed Enterobacteriaceae counts in pork of 3.38 log CFU/g, like those observed in this study. On the other hand, other studies have reported counts of 4.2 ± 0.99 log CFU/g in pork samples purchased in South Africa [63], higher than those found in the present investigation. The presence of Enterobacteriaceae has been related to improper handling of pork during processing [48].
In this study, various species of Enterobacteriaceae have been identified, with S. liquefaciens, R. aquatilis, and H. alvei standing out as the most prevalent among the isolated Enterobacteriaceae. Strains of Buttiauxella spp., P. agglomerans, K. oxytoca, E. americana, Serratia grimesii, and Y. enterocolitica have also been detected. Other researchers have reported the presence of Buttiauxella spp., P. agglomerans, Klebsiella pneumoniae, and Yersinia massiliensis in pork samples [60]. The presence of Y. enterocolitica is concerning, as it is associated with yersiniosis, an infection that may require hospitalization and, in severe cases, can be fatal for the infected individual [64]. Other studies have reported the presence of Y. enterocolitica strains in pork samples from Mexico, China, and Italy [65,66,67].
On the other hand, E. coli was not observed among the identified strains, although its presence in fresh pork meat acquired in Germany, China, France, and Italy has been described by other authors [60,61,68,69,70,71].
As for Staphylococcus spp. in our study, mean counts of 2.16 ± 0.74 log CFU/g were detected, a higher value than that found by Meng et al. [72] in pork samples in China (1.35 ± 0.33 log CFU/g) and Dorn-In et al. [61] in pork samples in Germany (1.5 log CFU/g).
In the present study, several strains of Kokuria spp. (K. palustris, K. rhizophila, and K. sasicia), Staphylococcus spp., and the species M. caseolyticus have been observed. Other studies also describe the presence of these bacteria in pork samples, coinciding with those found in our study, by detecting the presence of K. palustris, K. rhizophila, K. sasicia, M. caseolyticus, and strains of Staphylococcus spp. [60,61]. In a study carried out with fresh pork meat in Korea, Kocuria spp. as well as M. caseolyticus were isolated, coinciding with our results [73].
In the current research, six species of Staphylococcus spp. were found (S. aureus, S. epidermidis, S. equorum, S. saprophyticus, S. succinus, and S. warneri), as well as three species of Mammaliicococcus spp. (M. fleuretii, M. sciuri, and M. vitulinus), and the species M. caseolyticus. Other publications in Germany and Italy have described the identification of several species of Staphylococcus spp. isolated from pork meat, such as S. aureus, S. capitis, S. succinus, S. equorum, S. epidermidis, S. warneri, S. xylosus, S. chromogenes, S. haemolyticus, S. hominis, S. pasteuri, S. saprophyticus, and S. simulans, as well as the species M. caseolyticus [60,61]. These differences from our study could be due to the possibility of cross-contamination during carcass processing in slaughterhouses [74].
In the present study, phenotypic analysis was performed on 18 Staphylococcus spp. isolates, with only one identified as S. aureus. This strain was classified as methicillin-resistant and exhibited resistance to 8 different antibiotic families and 14 individual antibiotics. Other authors have reported the identification of 43 S. aureus strains out of a total of 99 pork samples in Oklahoma, which showed multi-resistance, with 100% resistance to ampicillin, 94.8% to tetracycline, 88.7% to penicillin, and 83.5% to doxycycline; 40.9% of the strains were classified as methicillin-resistant [29]. These findings contrast with those of the present study, where the S. aureus strain analyzed only showed resistance to tetracycline and penicillin among the antibiotics mentioned.
In a study conducted in Brazil using pork samples, 73 S. aureus strains were identified, 54 of which were classified as MRSA. Among these, 36.99% were resistant to tetracycline and 6.85% to vancomycin [32]. In contrast, in our study, all Staphylococcus spp. strains analyzed were susceptible to vancomycin. It is noteworthy that Staphylococcus spp. strains resistant to erythromycin (33.33%) were detected. Erythromycin is included in “Category B: restricted use in humans” of the Spanish National Action Plan on Antimicrobial Resistance [75]. The acquisition of infections through the consumption of food contaminated with bacteria resistant to antibiotics reserved for human use poses a serious threat to both human and animal health.
In this study, a strain of S. epidermidis was isolated that exhibited multidrug resistance to 5 antibiotic families and resistance to 6 antibiotics but it was not methicillin-resistant, while S. warneri was found to be resistant to 6 antibiotic families in addition to being methicillin-resistant. Other authors observed two strains of S. epidermidis isolated from pork, one resistant to ampicillin, cefoxitin, and gentamicin, and another strain resistant to cefoxitin, erythromycin, mupirocin, and tetracycline, both strains methicillin-resistant and multidrug-resistant against three and four antibiotic families, respectively [76].
Regarding the strains of Mammaliicococcus spp. and M. caseolyticus analyzed, two strains of M. caseolyticus and one of M. sciuri showed resistance to multiple drugs, and the strain of M. sciuri and one of the strains of M. caseolyticus were resistant to methicillin. Some authors have found strains of Mammaliicococcus spp. and M. caseolyticus isolated from pork resistant to antibiotics, but they do not specify against which ones [77,78]. No further studies describing the antibiotic sensitivity of Mammaliicococcus spp. and M. caseolyticus strains isolated from pork have been found. M. caseolyticus species and Mammaliicococcus spp. are closely related to Staphylococcus spp. and are potential disseminators of antibiotic resistance [34,79,80].
Snyder et al. [81] elucidated an average transfer of MRSA from contaminated pork products to cutting boards, ranging between 39% and 49%, depending on the type of product. Using an innovative dose–response colonization model for S. aureus proposed by Schoen et al. [82], the significant threat of the anticipated risk of nasal colonization by MRSA due to the handling of contaminated pork meat at the retail level was revealed. The identification of an MRSA isolate resistant to multiple antibiotics in pork meat samples raises a serious concern in terms of public health.
This finding highlights the importance of addressing and mitigating the spread of resistant strains in meat products not only from a human health perspective, but also from an animal and environmental health perspective, in accordance with the “One Health” paradigm. This approach allows for the implementation of faster and more targeted measures to tackle this issue [35].
In the present work, only phenotypic determination of methicillin-resistant Micrococcaceae was carried out. Since no molecular determination was undertaken, further studies are needed.

5. Conclusions

This study highlights that fresh pork meat can be a source of S. aureus resistant to methicillin (MRSA) and other antimicrobials. Moreover, pork meat can be a source of other multi-resistant strains belonging to the following species: S. succinus, M. sciuri, and M. caseolyticus. The presence of multi-resistant bacteria in fresh pork meat is of special concern. Additional measures should be taken within the framework of the “One Health” approach.

Author Contributions

A.M.-L.: methodology, investigation, data curation, formal analysis, writing—original draft. C.A.-F.: investigation, data curation. G.I.-T.: investigation. E.G.-F.: funding acquisition, project administration, conceptualization, methodology, data curation, formal analysis, visualization, investigation, supervision, writing—original draft preparation, writing—reviewing and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financed by Project FORTALECE 2021/05 financed by the Rioja Government (Spain).

Institutional Review Board Statement

Not applicable for studies not involving animals.

Informed Consent Statement

Not applicable for studies not involving animals.

Data Availability Statement

Data will be made available on request.

Acknowledgments

CAF acknowledges and extends her thanks to the University of La Rioja, the Rioja Government, and Santander for her predoctoral fellowship (UR-2024).

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
MRSAStaphylococcus aureus resistant to methicillin
MRSMethicillin-resistant staphylococci
MRMethicillin-resistant

References

  1. Biesalski, H.-K. Meat as a component of a healthy diet—Are there any risks or benefits if meat is avoided in the diet? Meat Sci. 2005, 70, 509–524. [Google Scholar] [CrossRef] [PubMed]
  2. Agarwal, S.; Fulgoni, V.L., 3rd. Association of pork (all pork, fresh pork and processed pork) consumption with nutrient intakes and adequacy in US children (age 2–18 years) and adults (age 19+ years): NHANES 2011–2018 analysis. Nutrients 2023, 15, 2293. [Google Scholar] [CrossRef] [PubMed]
  3. Walrand, S. Nutritional role of meat for children and adolescents. In Encyclopedia of Meat Sciences; Elsevier: Amsterdam, The Netherlands, 2024; pp. 655–662. [Google Scholar] [CrossRef]
  4. Conrad, Z.; Repoulis, V.; Zavela, C. Modeled sustainability impacts of increasing pork consumption among adults in the United States. Front. Nutr. 2025, 11, 1508601. [Google Scholar] [CrossRef] [PubMed]
  5. Mercasa. Alimentación en España 2022; Mercasa: Madrid, Spain, 2022; pp. 241–281. Available online: https://www.mercasa.es/publicaciones/alimentacion-en-espana/ (accessed on 29 April 2025).
  6. Taylor, T.M.; Aiyegoro, O.A. Microbial contamination: Microbial contamination of fresh meat. In Encyclopedia of Meat Sciences, 3rd ed.; Elsevier: Amsterdam, The Netherlands, 2024; Volume 2, pp. 181–188. [Google Scholar] [CrossRef]
  7. Alimi, B.A.; Lawal, R.; Odetunde, O.N. Food safety and microbiological hazards associated with retail meat at butchery outlets in north-central Nigeria. Food Control 2022, 139, 109061. [Google Scholar] [CrossRef]
  8. Hellstrom, S.; Laukkanen, R.; Siekkinen, K.M.; Ranta, J.; Mauala, R.; Korkeala, H. Listeria monocytogenes Contamination in Pork Can Originate from Farms. J. Food Prot. 2010, 73, 641–648. [Google Scholar] [CrossRef]
  9. Beneke, B.; Klees, S.; Stührenberg, 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]
  10. 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]
  11. Tan, L.K.; Ooi, P.T.; Thong, K.L. Prevalence of Yersinia enterocolitica from food and pigs in selected states of Malaysia. Food Control 2014, 35, 94–100. [Google Scholar] [CrossRef]
  12. Silva, D.A.L.; Botelho, C.V.; Martins, B.T.F.; Tavares, R.M.; Camargo, A.C.; Yamatogi, R.S.; Bersot, L.; Nero, L. Listeria monocytogenes from farm to fork in a Brazilian pork production chain. J. Food Prot. 2020, 83, 485–490. [Google Scholar] [CrossRef]
  13. Vico, J.P.; Lorenzutti, A.M.; Zogbi, A.P.; Aleu, G.; Sánchez, I.C.; Caffer, M.I.; Rosmini, M.R.; Mainar, R.C. Prevalence, associated risk factors, and antimicrobial resistance profiles of non-typhoidal Salmonella in large scale swine production in Córdoba, Argentina. Res. Vet. Sci. 2020, 130, 161–169. [Google Scholar] [CrossRef]
  14. Li, J.; Zhou, Y.; Yang, D.; Zhang, S.; Sun, Z.; Wang, Y.; Wangm, S.; Wu, C. Prevalence and antimicrobial susceptibility of Clostridium perfringens in chickens and pigs from Beijing and Shanxi, China. Vet. Microbiol. 2021, 252, 108932. [Google Scholar] [CrossRef] [PubMed]
  15. Linn, K.Z.; Furuta, M.; Nakayama, M.; Masuda, Y.; Honjoh, K.-I.; Miyamoto, T. Characterization and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from chicken and pork. Int. J. Food Microbiol. 2021, 360, 109440. [Google Scholar] [CrossRef]
  16. Haque, M.; Bosilevac, J.M.; Chaves, B.D. A review of Shiga-toxin producing Escherichia coli (STEC) contamination in the raw pork production chain. Int. J. Food Microbiol. 2022, 377, 109832. [Google Scholar] [CrossRef]
  17. Martins, B.T.F.; de Meirelles, J.L.; Omori, W.P.; de Oliveira, R.R.; Yamatogi, R.S.; Call, D.R.; Nero, L. Comparative genomics and antibiotic resistance of Yersinia enterocolitica obtained from a pork production chain and human clinical cases in Brazil. Food Res. Int. 2022, 152, 110917. [Google Scholar] [CrossRef]
  18. Sheng, H.; Suo, J.; Dai, J.; Wang, S.; Li, M.; Su, L.; Cao, M.; Cao, Y.; Chen, J.; Cui, S.; et al. Prevalence, antibiotic susceptibility and genomic analysis of Salmonella from retail meats in Shaanxi, China. Int. J. Food Microbiol. 2023, 403, 110305. [Google Scholar] [CrossRef]
  19. Lagarde, J.; Feurer, C.; Denis, M.; Douarre, P.-E.; Piveteau, P.; Roussel, S. Listeria monocytogenes prevalence and genomic diversity along the pig and pork production chain. Food Microbiol. 2024, 119, 104430. [Google Scholar] [CrossRef]
  20. Todd, E.C.D. Bacteria: Yersinia enterocolitica and Yersinia pseudotuberculosis. In Encyclopedia of Food Safety; Elsevier: Amsterdam, The Netherlands, 2014; pp. 574–580. [Google Scholar] [CrossRef]
  21. De Lucia, A.; Card, R.M.; Duggett, N.; Smith, R.P.; Davies, R.; Cawthraw, S.A.; Anjum, F. Reduction in antimicrobial resistance prevalence in Escherichia coli from a pig farm following withdrawal of group antimicrobial treatment. Vet. Microbiol. 2021, 258, 109125. [Google Scholar] [CrossRef]
  22. Bhargavi, D.; Sahu, R.; Nishanth, M.A.D.; Doijad, S.P.; Niveditha, P.; Kumar, O.R.V.; Sumanda, C. Genetic diversity and risk factor analysis of drug-resistant Escherichia coli recovered from broiler chicken farms. Comp. Immunol. Microbiol. Infect. Dis. 2023, 93, 101929. [Google Scholar] [CrossRef]
  23. Zomer, T.P.; Wielders, C.C.H.; Veenman, C.; Hengeveld, P.; van der Hoek, W.; de Greeff, S.C.; Smit, L. MRSA in persons not living or working on a farm in a livestock-dense area: Prevalence and risk factors. J. Antimicrob. Chemother. 2017, 72, 893–899. [Google Scholar] [CrossRef] [PubMed]
  24. Ou, C.; Shang, D.; Yang, J.; Chen, B.; Chang, J.; Jin, F.; Shi, C. Prevalence of multidrug-resistant Staphylococcus aureus isolates with strong biofilm formation ability among animal-based food in Shanghai. Food Control 2020, 112, 107106. [Google Scholar] [CrossRef]
  25. Tegegne, H.A.; Koláčková, I.; Florianová, M.; Gelbíčová, T.; Madec, J.-Y.; Haenni, M.; Karpíšková, R. Detection and molecular characterisation of methicillin-resistant Staphylococcus aureus isolated from raw meat in the retail market. J. Glob. Antimicrob. Resist. 2021, 26, 233–238. [Google Scholar] [CrossRef]
  26. Ribeiro, C.M.; Stefani, L.M.; Lucheis, S.B.; Okano, W.; Cruz, J.C.M.; Souza, G.V.; Casagrande, T. Methicillin-resistant Staphylococcus aureus in poultry and poultry meat: A meta-analysis. J. Food Prot. 2018, 81, 1055–1062. [Google Scholar] [CrossRef]
  27. Tsai, H.-C.; Hsu, B.-M.; Koner, S.; Chen, J.-S.; Hsu, G.-J.; Rathod, J.; Kenneth, M. The molecular classification of methicillin-resistant Staphylococcus aureus (MRSA) clones in the livestock settings air, and their potential bioaerosol-based transmission risk to the ambient environment: A challenge to One-health approach. J. Aerosol Sci. 2024, 179, 106381. [Google Scholar] [CrossRef]
  28. Tuominen, K.S.; Sternberg Lewerin, S.; Widgren, S.; Rosendal, T. Assessment of control measures against livestock-associated methicillin-resistant Staphylococcus aureus in a farrow-to-finish pig herd using infectious disease modelling. Animal 2023, 17, 100840. [Google Scholar] [CrossRef]
  29. 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]
  30. Ge, B.; Mukherjee, S.; Hsu, C.-H.; Davis, J.A.; Tran, T.T.T.; Yang, Q.; Abbot, J. MRSA and multidrug-resistant Staphylococcus aureus in U.S. retail meats, 2010-2011. Food Microbiol. 2017, 62, 289–297. [Google Scholar] [CrossRef]
  31. Sun, C.; Chen, B.; Hulth, A.; Schwarz, S.; Ji, X.; Nilsson, L.E.; Ma, S. Genomic analysis of Staphylococcus aureus along a pork production chain and in the community, Shandong Province, China. Int. J. Antimicrob. Agents 2019, 54, 8–15. [Google Scholar] [CrossRef]
  32. Nero, L.A.; Botelho, C.V.; Sovinski, Â.I.; Grossi, J.L.; Call, D.R.; Dos Santos Bersot, L. Occurrence and distribution of antibiotic-resistant Staphylococcus aureus in a Brazilian pork production chain. J. Food Prot. 2022, 85, 973–979. [Google Scholar] [CrossRef]
  33. González-Machado, C.; Alonso-Calleja, C.; Capita, R. Prevalence and types of methicillin-resistant Staphylococcus aureus (MRSA) in meat and meat products from retail outlets and in samples of animal origin collected in farms, slaughterhouses and meat processing facilities. A review. Food Microbiol. 2024, 123, 104580. [Google Scholar] [CrossRef]
  34. Nemeghaire, S.; Vanderhaeghen, W.; Argudín, M.A.; Haesebrouck, F.; Butaye, P. Characterization of methicillin-resistant Staphylococcus sciuri isolates from industrially raised pigs, cattle and broiler chickens. J. Antimicrob. Chemother. 2014, 69, 2928–2934. [Google Scholar] [CrossRef]
  35. Cuny, C.; Layer-Nicolaou, F.; Werner, G.; Witte, W. A look at staphylococci from the one health perspective. Int. J. Med. Microbiol. 2024, 314, 151604. [Google Scholar] [CrossRef]
  36. European Food Safety Authority (EFSA); European Centre for Disease Prevention and Control (ECDC). The European Union One Health 2022 Zoonoses Report. EFSA J. 2023, 21, e08442. [Google Scholar] [CrossRef]
  37. Pinamonti, D.; Manzano, M.; Maifreni, M.; Bianco, S.; Domi, B.; Ferrin, A. Prevalence and characterization of Staphylococcus aureus isolated from meat and milk in Northeastern Italy. J. Food Prot. 2025, 88, 100442. [Google Scholar] [CrossRef]
  38. Kisoo, L.; Muloi, D.M.; Oguta, W.; Ronoh, D.; Kirwa, L.; Akoko, J. Practices and drivers for antibiotic use in cattle production systems in Kenya. One Health 2023, 17, 100646. [Google Scholar] [CrossRef]
  39. Courtioux, B. Le concept One Health, un changement de paradigme. Actual. Pharm. 2024, 63, 40–43. [Google Scholar] [CrossRef]
  40. Agencia Española de Medicamentos y Productos Sanitarios (AEMPS). Informe del Plan Nacional Frente a la Resistencia a los Antibióticos (PRAN) 2022–2023; Plan Nacional Frente a la Resistencia a los Antibióticos (PRAN): Madrid, Spain, 2023; Available online: https://resistenciaantibioticos.es/sites/default/files/2025-01/Informe%20anual%20PRAN%202022-2023.pdf (accessed on 29 April 2025).
  41. Serrano, M.J.; Elorduy, J.; Zabaleta, I.; Istamboulie, G.; González-Fandos, E.; Bousquet-Mélou, A.; Mata, L.; Aymard, C.; Martínez-Laorden, A.; Da Silva-Guedes, J.; et al. Antimicrobial residue assessment in 5357 commercialized meat samples from the Spain-France cross-border area: A new approach for effective monitoring. Food Control 2022, 138, 109033. [Google Scholar] [CrossRef]
  42. Ministerio de Agricultura, Pesca y Alimentación. Informe del Consumo de Alimentación en España 2019; MAPA: Madrid, Spain, 2019. [Google Scholar]
  43. Martínez-Laorden, A.; Arraiz-Fernández, C.; González-Fandos, E. Microbiological quality and safety of fresh turkey meat at retail level, including the presence of ESBL-producing Enterobacteriaceae and methicillin-resistant S. aureus. Foods 2023, 12, 1274. [Google Scholar] [CrossRef]
  44. Martinez-Laorden, A.; Arraiz-Fernandez, C.; Gonzalez-Fandos, E. Microbiological quality and safety of fresh quail meat at the retail level. Microorganisms 2023, 11, 2213. [Google Scholar] [CrossRef]
  45. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing, 30th ed.; CLSI Document M 100; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2020. [Google Scholar]
  46. Ekonomou, S.I.; Leech, D.J.; Lightfoot, S.; Huson, D.; Stratakos, A.C. Development of novel antimicrobial coatings incorporating linalool and eugenol to improve the microbiological quality and safety of raw chicken. Lebenson Wiss. Technol. 2023, 182, 114839. [Google Scholar] [CrossRef]
  47. Alessandroni, L.; Caprioli, G.; Faiella, F.; Fiorini, D.; Galli, R.; Huang, X.; Marinelli, G. A shelf-life study for the evaluation of a new biopackaging to preserve the quality of organic chicken meat. Food Chem. 2022, 371, 131134. [Google Scholar] [CrossRef]
  48. Yan, Y.; Zhu, X.; Lu, A.; Yang, X.; Yu, J.; Qu, J. Effect of 60Co-γ-irradiation on the degradation of β-agonists residues and the quality of fresh pork during refrigeration. Food Control 2024, 160, 110362. [Google Scholar] [CrossRef]
  49. Beltrán-Cotta, L.A.; Passos, R.S.F.T.; Costa, N.P.; Barreto, B.G.; Veloso, A.C.; da Silva, M.C.A.; Costa, M. Use of yellow mombin (Spondias mombin L.) in marination: Effect on quality properties of Boston butt pork during refrigerated storage. Meat Sci. 2023, 204, 109257. [Google Scholar] [CrossRef]
  50. Duranton, F.; Guillou, S.; Simonin, H.; Chéret, R.; de Lamballerie, M. Combined use of high pressure and salt or sodium nitrite to control the growth of endogenous microflora in raw pork meat. Innov. Food Sci. Emerg. Technol. 2012, 16, 373–380. [Google Scholar] [CrossRef]
  51. Rodrigues, D.; Flores, D.R.M.; da Silva, J.S.; Genro, A.L.G.; Silva, M.S.; Klein, B.; Mello, E. Application of electrolyzed water for improving pork meat quality. Food Res. Int. 2017, 100 Pt 1, 757–763. [Google Scholar] [CrossRef]
  52. Yimenu, S.M.; Koo, J.; Kim, B.S.; Kim, J.H.; Kim, J.Y. Freshness-based real-time shelf-life estimation of packaged chicken meat under dynamic storage conditions. Poult. Sci. 2019, 98, 6921–6930. [Google Scholar] [CrossRef]
  53. Zhou, Z.; Ren, F.; Huang, Q.; Cheng, H.; Cun, Y.; Ni, Y.; Wu, W. Characterization and interactions of spoilage of Pseudomonas fragi C6 and Brochothrix thermosphacta S5 in chilled pork based on LC-MS/MS and screening of potential spoilage biomarkers. Food Chem. 2024, 444, 138562. [Google Scholar] [CrossRef]
  54. Papadopoulou, O.; Panagou, E.Z.; Tassou, C.C.; Nychas, G.-J.E. Contribution of Fourier transform infrared (FTIR) spectroscopy data on the quantitative determination of minced pork meat spoilage. Food Res. Int. 2011, 44, 3264–3271. [Google Scholar] [CrossRef]
  55. Tang, Y.-F.; Lin, Y.-S.; Su, L.-H.; Liu, J.-W. Increasing trend of healthcare-associated infections due to vancomycin-resistant Enterococcus faecium (VRE-fm) paralleling escalating community-acquired VRE-fm infections in a medical center implementing strict contact precautions: An epidemiologic and pathogenic genotype analysis and its implications. J. Microbiol. Immunol. Infect. 2023, 56, 1045–1053. [Google Scholar] [CrossRef]
  56. Kulawik, P.; Jamróz, E.; Tkaczewska, J.; Vlčko, T.; Zając, M.; Guzik, P.; Janik, M. pplication of antimicrobial chitosan-Furcellaran-hydrolysate gelatin edible coatings enriched with bioactive peptides in shelf-life extension of pork loin stored at 4 and −20 °C. Int. J. Biol. Macromol. 2024, 254 Pt 2, 127865. [Google Scholar] [CrossRef]
  57. Liang, R.; Zhang, W.; Mao, Y.; Zhang, Y.; Li, K.; Luo, X.; Yang, X. Effects of CO2 on the physicochemical, microbial, and sensory properties of pork patties packaged under optimized O2 levels. Meat Sci. 2024, 209, 109422. [Google Scholar] [CrossRef]
  58. Stellato, G.; Utter, D.R.; Voorhis, A.; De Angelis, M.; Eren, A.M.; Ercolini, D. A few Pseudomonas oligotypes dominate in the meat and dairy processing environment. Front. Microbiol. 2017, 8, 264. [Google Scholar] [CrossRef] [PubMed]
  59. Gong, J.; Liu, S.; Wang, H.; Shao, L.; Chen, S.; Xu, X.; Wang, H. Investigating meat-borne bacterial profiles related to biofilm formation: An in situ and in vitro assessment. Food Control 2024, 157, 110175. [Google Scholar] [CrossRef]
  60. Peruzy, M.F.; Houf, K.; Joossens, M.; Yu, Z.; Proroga, Y.T.R.; Murru, N. Evaluation of microbial contamination of different pork carcass areas through culture-dependent and independent methods in small-scale slaughterhouses. Int. J. Food Microbiol. 2021, 336, 108902. [Google Scholar] [CrossRef]
  61. Dorn-In, S.; Mang, S.; Cosentino, R.O.; Schwaiger, K. Changes in the Microbiota from fresh to spoiled meat, determined by culture and 16S rRNA analysis. J. Food Prot. 2024, 87, 100212. [Google Scholar] [CrossRef] [PubMed]
  62. Chandrasekar, C.M.; Nespoli, L.; Bellesia, T.; Ghaani, M.; Farris, S.; Romano, D. Fabrication of double layer nanoparticle infused starch-based thermoplastic food packaging system for meat preservation. Int. J. Biol. Macromol. 2024, 254 Pt 1, 127689. [Google Scholar] [CrossRef] [PubMed]
  63. Magqupu, S.; Katiyatiya, C.L.F.; Chikwanha, O.C.; Strydom, P.E.; Mapiye, C. Quality and safety of pork sold in the informal urban street markets of the Cape Metropole, South Africa. Meat Sci. 2023, 204, 109270. [Google Scholar] [CrossRef]
  64. Wang, H.; Zheng, Y.; Ren, H.-L.; Xiao, Y.-R.; Wang, C.; Chang, J.; Wuong, Y. A lateral flow immunochromatographic strip based on RPA and quantum dot nanobeads for rapid identification of pathogenic Yersinia enterocolitica. Lebenson Wiss. Technol. 2023, 187, 115271. [Google Scholar] [CrossRef]
  65. Quiñonez, E.I.; Vázquez-Salinas, C.; Rodas-Suárez, O.R.; Pedroche, F.F. Isolation of Yersinia from raw meat (pork and chicken) and precooked meat (porcine tongues and sausages) collected from commercial establishments in Mexico City. J. Food Prot. 2000, 63, 542–544. [Google Scholar] [CrossRef]
  66. Bonardi, S.; Paris, A.; Bassi, L.; Salmi, F.; Bacci, C.; Riboldi, E.; Boni, E. Detection, semiquantitative enumeration, and antimicrobial susceptibility of Yersinia enterocolitica in pork and chicken meats in Italy. J. Food Prot. 2010, 73, 1785–1792. [Google Scholar] [CrossRef]
  67. Gao, H.; Lei, Z.; Jia, J.; Wang, S.; Chen, Y.; Sun, M.; Kiang, C. Application of loop-mediated isothermal amplification for detection of Yersinia enterocolitica in pork meat. J. Microbiol. Methods 2009, 77, 198–201. [Google Scholar] [CrossRef]
  68. Bouvet, J.; Bavai, C.; Rossel, R.; Le Roux, A.; Montet, M.P.; Ray-Gueniot, S.; Mazui, B. Effects of cutting process on pork meat contamination by verotoxin-producing Escherichia coli (VTEC) and E. coli O157:H7. Int. J. Food Microbiol. 2002, 77, 91–97. [Google Scholar] [CrossRef] [PubMed]
  69. Schwaiger, K.; Huther, S.; Hölzel, C.; Kämpf, P.; Bauer, J. Prevalence of antibiotic-resistant enterobacteriaceae isolated from chicken and pork meat purchased at the slaughterhouse and at retail in Bavaria, Germany. Int. J. Food Microbiol. 2012, 154, 206–211. [Google Scholar] [CrossRef] [PubMed]
  70. Rega, M.; Andriani, L.; Poeta, A.; Casadio, C.; Diegoli, G.; Bonardi, S.; Conter, M. Transmission of β-lactamases in the pork food chain: A public health concern. One Health 2023, 17, 100632. [Google Scholar] [CrossRef]
  71. Wang, Y.; Qu, M.; Bi, Y.; Liu, W.J.; Ma, S.; Wan, B.; Hu, Y. The multi-kingdom microbiome catalog of the chicken gastrointestinal tract. Biosaf. Health 2024, 6, 101–115. [Google Scholar] [CrossRef]
  72. Meng, D.-M.; Sun, S.-N.; Shi, L.-Y.; Cheng, L.; Fan, Z.-C. Application of antimicrobial peptide mytichitin-CB in pork preservation during cold storage. Food Control 2021, 125, 108041. [Google Scholar] [CrossRef]
  73. Kim, Y.; Ban, G.-H.; Hong, Y.W.; Jeong, K.C.; Bae, D.; Kim, S.A. Bacterial profile of pork from production to retail based on high-throughput sequencing. Food Res. Int. 2024, 176, 113745. [Google Scholar] [CrossRef]
  74. Pletinckx, L.J.; Verhegghe, M.; Dewulf, J.; Crombé, F.; De Bleecker, Y.; Rasschaert, G.; Goddeeris, B.M.; Manm, I. Screening of poultry-pig farms for methicillin-resistant Staphylococcus aureus: Sampling methodology and within herd prevalence in broiler flocks and pigs. Infect. Genet. Evol. 2011, 11, 2133–2137. [Google Scholar] [CrossRef]
  75. Plan Nacional frente a la Resistencia a los Antibióticos (PRAN). Categorización de Antibióticos; PRAN: Madrid, Spain, 2023; Available online: https://resistenciaantibioticos.es/es/lineas-de-accion/vigilancia/antibioticos-criticos (accessed on 22 April 2025).
  76. Lee, G.Y.; Lee, H.H.; Yang, S.-J. Antimicrobial resistance profiles and clonal diversity of Staphylococcus epidermidis isolates from pig farms, slaughterhouses, and retail pork. Vet. Microbiol. 2023, 282, 109753. [Google Scholar] [CrossRef] [PubMed]
  77. Li, L.; Heidemann Olsen, R.; Ye, L.; Yan, H.; Nie, Q.; Meng, H.; Shi, L. Antimicrobial resistance and resistance genes in aerobic bacteria isolated from pork at slaughter. J. Food Prot. 2016, 79, 589–597. [Google Scholar] [CrossRef]
  78. Shang, Y.; Zhang, Y.; Li, S.; Jia, Y.; Ma, A. Analysis of contamination with drug-resistant bacteria among three types of commercially available pork in Beijing and Shanxi, China. Lebenson Wiss. Technol. 2023, 187, 115272. [Google Scholar] [CrossRef]
  79. Mazhar, S.; Hill, C.; McAuliffe, O. The genus Macrococcus: An insight into its biology, evolution, and relationship with Staphylococcus. Adv. Appl. Microbiol. 2018, 105, 1–50. [Google Scholar] [CrossRef] [PubMed]
  80. Keller, J.E.; Schwendener, S.; Neuenschwander, J.; Overesch, G.; Perreten, V. Prevalence and characterization of methicillin-resistant Macrococcus spp. in food producing animals and meat in Switzerland in 2019. Schweiz. Arch. Für Tierheilkd. 2021, 164, 153–164. [Google Scholar] [CrossRef]
  81. Snyder, H.L.; Niebuhr, S.E.; Dickson, J.S. Transfer of methicillin-resistant Staphylococcus aureus from retail pork products onto food contact surfaces and the potential for consumer exposure. J. Food Prot. 2013, 76, 2087–2092. [Google Scholar] [CrossRef] [PubMed]
  82. Schoen, M.E.; Peckham, T.K.; Shirai, J.H.; Kissel, J.C.; Thapaliya, D.; Smith, T.C.; Scott, J. Risk of nasal colonization of methicillin-resistant Staphylococcus aureus during preparation of contaminated retail pork meat. Microb. Risk Anal. 2020, 16, 100136. [Google Scholar] [CrossRef]
Table 1. Microbiological load (log CFU/g) detected in 39 samples of fresh pork meat.
Table 1. Microbiological load (log CFU/g) detected in 39 samples of fresh pork meat.
Microbial GroupN 1 Counts < 1 log CFU/gN Counts > 1 Log CFU/gMinimum Value (log CFU/g)Maximum Value (log CFU/g)Mean ± Standard Deviation
Mesophiles0392.007.454.93 ± 1.37
Pseudomonas19202.006.153.89 ± 1.17
Enterobacteriaceae25141.604.493.46 ± 0.86
Staphylococci24151.303.922.16 ± 0.74
1 Number of samples.
Table 2. Bacterial species isolated from PCA in fresh pork meat.
Table 2. Bacterial species isolated from PCA in fresh pork meat.
Microbial Group
(N 1; Percentage)		SpecieNumber of StrainsPercentage (%)
Pseudomonas spp.
(25; 22.12%)		Pseudomonas extremorientalis10.88
Pseudomonas fragi1412.39
Pseudomonas libanensis10.88
Pseudomonas lundensis97.96
Micrococcaceae
(14; 12.39%)		Kocuria palustris10.88
Kocuria rhizophila65.31
Kocuria salsicia43.54
Macrococcus caseolyticus10.88
Staphylococcus warneri21.77
BAL
(22; 19.47%)		Carnobacterium divergens1614.16
Carnobacterium maltaromaticum32.65
Lactobacillus sp.21.77
Lactococcus lactis10.88
Enterobacteriacecae
(10; 8.85%)		Citrobacter braakii10.88
Hafnia alvei32.65
Rahnella inusitata43.54
Serratia proteamaculans21.77
Brochothrix thermosphacta
(30; 26.55%)		Brochothrix thermosphacta3026.55
Other Gram-negative bacteria
(9; 7.96%)		Acinetobacter guillouiae21.77
Acinetobacter harbinensis43.54
Acinetobacter lactucae10.88
Stenotrophomonas rhizophila10.88
Moraxella osloensis10.88
Other Gram-positive bacteria
(3; 2.65%)		Dermacoccus nishinomiyaensis32.65
1 Number of strains isolated.
Table 3. Bacterial species isolated from specific media in fresh pork meat.
Table 3. Bacterial species isolated from specific media in fresh pork meat.
Media (N 1)SpeciesNumber of StrainsPercentage (%)
Chromogenic Pseudomonas Agar (78)Pseudomonas antarctica78.97
Pseudomonas azotoformans810.26
Pseudomonas extremorientalis56.41
Pseudomonas fluorescens1114.10
Pseudomonas fragi22.56
Pseudomonas libanensis3241.03
Pseudomonas marginalis22.56
Pseudomonas poae11.28
Pseudomonas rhodesiae11.28
Pseudomonas synxantha33.85
Pseudomonas tolaasii11.28
Pseudomonas trivialis11.28
Pseudomonas veronii45.13
MacConkey Agar (65)Buttiauxella gaviniae34.62
Buttiauxella warmboldiae57.69
Ewingella americana57.69
Hafnia alvei913.85
Klebsiella oxytoca34.62
Pantoea agglomerans34.62
Rahnella aquatilis1320.00
Serratia grimesii23.08
Serratia liquefaciens2132.31
Yersinia enterocolitica11.54
Mannitol Salt Agar (49)Kocuria uropygioeca12.04
Macrococcus caseolyticus612.24
Mammaliicoccus fleurettii12.04
Mammaliicoccus sciuri48.16
Mammaliicoccus vitulinus36.12
Staphylococcus epidermidis24.08
Staphylococcus equorum510.20
Staphylococcus saprophyticus1938.78
Staphylococcus succinus24.08
Staphylococcus warneri612.24
1 Number of strains isolated.
Table 4. Antimicrobial resistance phenotypic profile of Staphylococcus spp., Mammaliicoccus spp., and Macrococcus caseolyticus strains isolated from fresh pork meat.
Table 4. Antimicrobial resistance phenotypic profile of Staphylococcus spp., Mammaliicoccus spp., and Macrococcus caseolyticus strains isolated from fresh pork meat.
IdentificationPhenotypic Pattern of Resistance 1Multirresist 2MR 3
Staphylococcus aureusAK-S-K-TOB-FOX-CMN-MY-PNG-P-SUZ-MH-TE-FAD-PUM CYes (8) 5Yes
Staphylococcus epidermidisTOB-ERY-P-SUZ-DO-TE BYes (5)No
- 4BNoNo
Staphylococcus equorumERY-W BNoNo
MY-ERY BNoNo
- BNoNo
Staphylococcus saprophyticusERY-FAD BNoNo
PNG-P-DO-TE BNoNo
- BNoNo
- BNoNo
- BNoNo
DO-TE BNoNo
Staphylococcus succinus- BNoNo
- BNoNo
Staphylococcus warneriS-TOB-FOX-P-SUZ-FAD-PUM BYes (6)Yes
ERY ANoNo
MY-P BNoNo
ERY ANoNo
Mammaliicoccus fleurettiiMY BNoNo
Mammaliicoccus sciuriMY-FAD BNoNo
FOX-MY-P-PUM BYes (4) 5Yes
Mammaliicoccus vitulinus- BNoNo
MY BNoNo
Macrococcus caseolyticusCMN-MY-ERY-TE BYes (3) 4No
MY-ERY BNoNo
MY-ERY ANoNo
AK-FOX-CPT-MY-P-PUM BYes (5)Yes
1 The letters indicate the isolation medium. A Agar Plate Count. B Agar Manitol Sal. C ChromID MRSA. 2 Multidrug resistance. 3 Methicillin-resistant. 4 Susceptible to all the antibiotics tested. 5 Number of antibiotic families to which the strain is resistant. AK: amikacin, S: streptomycin, K: kanamycin, TOB: tobramycin, FOX: cefoxitin, CMN: clindamycin, MY: lincomycin, ERY: erythromycin, P: penicillin, SUZ: sulfadiazine, DO: doxycycline, MH: minocycline, TE: tetracycline, FAD: fusidic acid, PUM: mupirocin, W: trimethoprim, PNG: benzylpenicillin.
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Martinez-Laorden, A.; Arraiz-Fernandez, C.; Ibañez-Torija, G.; Gonzalez-Fandos, E. Microbiological Quality and Safety of Fresh Pork Meat with Special Reference to Methicillin-Resistant S. aureus and Other Staphylococci. Vet. Sci. 2025, 12, 568. https://doi.org/10.3390/vetsci12060568

AMA Style

Martinez-Laorden A, Arraiz-Fernandez C, Ibañez-Torija G, Gonzalez-Fandos E. Microbiological Quality and Safety of Fresh Pork Meat with Special Reference to Methicillin-Resistant S. aureus and Other Staphylococci. Veterinary Sciences. 2025; 12(6):568. https://doi.org/10.3390/vetsci12060568

Chicago/Turabian Style

Martinez-Laorden, Alba, Celia Arraiz-Fernandez, Gonzalo Ibañez-Torija, and Elena Gonzalez-Fandos. 2025. "Microbiological Quality and Safety of Fresh Pork Meat with Special Reference to Methicillin-Resistant S. aureus and Other Staphylococci" Veterinary Sciences 12, no. 6: 568. https://doi.org/10.3390/vetsci12060568

APA Style

Martinez-Laorden, A., Arraiz-Fernandez, C., Ibañez-Torija, G., & Gonzalez-Fandos, E. (2025). Microbiological Quality and Safety of Fresh Pork Meat with Special Reference to Methicillin-Resistant S. aureus and Other Staphylococci. Veterinary Sciences, 12(6), 568. https://doi.org/10.3390/vetsci12060568

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