Next Article in Journal
Microbiota Assessment of Fresh-Cut Apples Packaged in Two Different Films
Next Article in Special Issue
Identification of Fungicide Combinations Targeting Plasmopara viticola and Botrytis cinerea Fungicide Resistance Using Machine Learning
Previous Article in Journal
Bacterial Microbiota of Asthmatic Children and Preschool Wheezers’ Airways—What Do We Know?
Previous Article in Special Issue
Genomic Characterization of Multidrug-Resistant Extended Spectrum β-Lactamase-Producing Klebsiella pneumoniae from Clinical Samples of a Tertiary Hospital in South Kivu Province, Eastern Democratic Republic of Congo
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Microorganisms
Volume 11
Issue 5
10.3390/microorganisms11051155
microorganisms-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:
Article

Prevalence of mecA and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Clinical Isolates from Gaza Strip Hospitals

by
Nabil Abdullah El Aila
1,*,
Nahed Ali Al Laham
2 and
Thierry Naas
3,4,5,*
1
Department of Medical Laboratory Sciences, Faculty of Medical Sciences, Al-Aqsa University Gaza, Gaza P.O. Box 405, Palestine
2
Department of Laboratory Medicine, Faculty of Medical Sciences, Al-Azhar University-Gaza, Gaza P.O. Box 1277, Palestine
3
Bacteriology-Hygiene Unit, Hôpital Bicêtre, AP-HP Paris-Saclay, 94270 Le Kremlin-Bicêtre, France
4
Faculty of Medicine, Team ReSIST, UMR1184, INSERM, CEA, Université Paris-Saclay, 94270 Le Kremlin-Bicêtre, France
5
French National Reference Center for Antimicrobial Resistances, Hôpital Bicêtre, AP-HP Paris-Saclay, 94270 Le Kremlin-Bicêtre, France
*
Authors to whom correspondence should be addressed.
Microorganisms 2023, 11(5), 1155; https://doi.org/10.3390/microorganisms11051155
Submission received: 17 January 2023 / Revised: 24 April 2023 / Accepted: 26 April 2023 / Published: 28 April 2023
(This article belongs to the Special Issue Advances in Antibiotic and Drug-Resistance Mechanisms)
Review Reports Versions Notes

Abstract

:
Methicillin-resistant Staphylococcus aureus (MRSA) are spreading worldwide in hospital and community settings, thus posing a serious public health problem. Panton-Valentine Leukocidin (PVL), an important virulence factor of S. aureus, is a marker of community-acquired MRSA. Here we determined the prevalence of pvl genes among S. aureus isolates from different hospitals in the Gaza Strip, Palestine. A total of 285 S. aureus isolates were collected from five different hospitals in the Gaza Strip. All isolates were characterized for their susceptibility patterns to available antimicrobial agents and by using multiplex PCR for the detection of mecA and pvl genes. The overall prevalence of MRSA in Gaza hospitals was 70.2% (range: 76.3% to 65.5%) and that of pvl among S. aureus isolates was 29.8% (range: 32.9% to 26.2%). The pvl gene was equally prevalent among MRSA isolates (30.5%) and MSSA isolates (28.2%). The most effective antibiotics were rifampicin, vancomycin, and clindamycin, with susceptibility rates of 91.2%, 88.7%, and 84.6%, respectively. The highest percentage of strains were observed to be resistant to penicillin and amoxicillin with clavulanic acid—96.1% and 73.6%, respectively. Our results showed a high prevalence of MRSA and pvl-positive isolates in Gaza Strip hospitals, which likely reflects the situation in the community. It is mandatory to implement systematic surveillance of both hospital and community isolates, together with interventions (such as increased hand hygiene, use of hydroalcoholic solutions, and isolation of carriers) to limit their spread.

1. Introduction

Staphylococcus aureus (SA) is a major human pathogen that causes infections ranging from minor skin and soft tissue infections to life-threatening sepsis. It has been linked to both community-acquired (CA) and healthcare-associated (HA) infections, both of which cause significant morbidity and mortality [1,2,3,4]. Methicillin-Resistant SA (MRSA) isolates were initially identified in 1961 and have since become major nosocomial pathogens worldwide [5]. Methicillin resistance developed because of the acquisition of a mobile genetic element known as staphylococcal cassette chromosome mec (SCCmec), which contains the mecA resistance gene that encodes a penicillin-binding protein variant (PBP2a) with a lower affinity for β-lactam antibiotics [6]. A new variant of mecA, known as mecC (initially referred to as mecALGA251), has been discovered in MRSA samples collected from humans and various animal species, including livestock, small mammals, and birds in Europe. This type of mec bears 70% similarity in terms of nucleotide identity with mecA (Harrison et al., 2014).
The ability of MRSA to cause various infections is primarily due to the presence of toxins and various extracellular and surface virulence factors with adhesive properties, such as Panton-Valentine Leukocidin (PVL) [7]. By creating pores in the mitochondrial membrane, PVL destroys leukocytes and alters the immune system, ultimately leading to mitochondrial cell membrane lysis and death [8,9]. The PVL toxin is responsible for skin and soft tissue infections, necrotizing pneumonia, diffuse cellulitis, and osteomyelitis [10]. Patients with PVL-positive MRSA infection had a higher mortality rate [11]. Although the prevalence of PVL-producing S. aureus isolates varies across the globe, increasing reports signal that the increase in PVL-positive MRSA constitutes a significant public health challenge [12].
Epidemiological and clinical data show that CA-MRSA isolates with high virulence potential express PVL [13,14], which has also been shown to be an important contributing factor in CA-MSSA infections, especially in severe skin and soft tissue infections (SSTI) and, most remarkably, necrotizing pneumonia [15,16,17]. The pvl genes were discovered in cutaneous and invasive infections carried by HA-MRSA strains [18]. According to the published data in Palestine, the prevalence of resistance to methicillin among S. aureus strains isolated from hospitalized patients is steadily increasing [19,20,21,22,23]. However, only a few studies in Palestine, and almost none in the Gaza Strip, addressed the prevalence and clonal spread of PVL-producing S. aureus isolated from patients in Palestine.
Our study aims to provide insights into the molecular characteristics of PVL-producing S. aureus strains and antibiotic resistance phenotypes considering the increasing prevalence of Multidrug-Resistant (MDR)-PVL-positive MRSA and its spread in Gaza Strip hospitals.

2. Materials and Methods

2.1. Study Design

The Gaza Strip (31°250 N, 34°200 E) is a narrow territory along the eastern Mediterranean coast (41 km long and 6–12 km wide), with tightly controlled borders abutting Israel and Egypt’s Sinai Peninsula. It is regarded as one of the world’s most densely populated areas, with a population of approximately 2.1 million inhabitants (37.5% of the total estimated Palestinian population) and a population density (4073/km2) nearly ten times greater than that of the West Bank (433/km2) [24].
The study was set out as a cross-sectional study in five different hospitals in the Gaza Strip.
Two-hundred and eighty-five S. aureus isolates were collected from different clinical samples including pus, blood, sputum, urine, nasal, and ear swab samples between July 2019–December 2019. The study was approved by the department of human resources and development in the Ministry of Health—Gaza, Palestine under study approval number PHRC/HC/227/17.

2.2. Sample Collection and Phenotypic Detection of S. aureus

In each hospital involved in this study, S. aureus isolates were collected and identified using morphological (Gram stain), biochemical (Coagulase, Mannitol salt agar, and DNase) methods. To confirm the fermentation of mannitol, the growth of yellow colonies on Mannitol salt agar (HiMedia, Mumbai, India) surrounded by yellow zones after 24 h of incubation at 37 °C indicated a positive result [25]. For tube coagulase tests, colonies of test isolates were re-suspended in 2 mL of citrated human plasma in sterile glass test tubes. The tubes were incubated at 35 °C for 4 h and observed for clot formation. The DNase test was performed by inoculating Staph isolates on deoxyribonuclease (DNase) agar (HiMedia, Mumbai, India) and incubated for 24 h at 37 °C. An excess of 1 N HCl (about 15 mL) was then added. A vacuum pipette was used to remove extra acid and clear areas around the bacterial colonies revealed DNase-positive colonies [25]. The isolates were kept in trypticase soy agar until further investigation. Confirmation of identification and antibiotic susceptibility testing of the S. aureus strains was carried out in the microbiology laboratory of Al Aqsa University in the Gaza Strip, Palestine.

2.3. DNA Extraction and Molecular Detection of mecA Gene and lukS/F-PV Gene by PCR

DNA was extracted from cultured isolates using alkaline lysis, as previously described [26,27]. In brief, one bacterial colony was suspended in 20 µL of lysis buffer (0.25% sodium dodecyl sulfate, 0.05 N NaOH) and heated for 15 min at 95 °C. A total of 180 µL of distilled water was used to dilute the cell lysate. The cell debris was centrifuged at 16,000× g for 5 min, and the supernatants were used for PCR or stored at −20 °C until further use. Extracted DNA from the different isolates was used in a multiplex PCR assay that detects three genes: the 16SrRNA gene used as an internal control, the mecA gene for MRSA detection, and the lukS/F-PV gene for PVL detection [27]. Two control strains, the S. aureus ATCC 25923 (carrying the pvl gene) and S. aureus ATCC 33592 (carrying the mecA gene), were added in each run.
Thermal cycling conditions were set at 94 °C for 10 min followed by 10 cycles of 94 °C for 45 s, 55 °C for 45 s, and 72 °C for 75 s and 25 cycles of 94 °C for 45 s, 50 °C for 45 s, and 72 °C for 75 s. PCR products were analyzed on 1.5% agarose gel containing 2 µL ethidium bromide (0.5 µg/mL). The primers are listed in Table 1 [27].

2.4. Antimicrobial Susceptibility Testing

Antibiotic susceptibility testing was performed following the Kirby Bauer disc diffusion method as recommended by CLSI guidelines [28] using Mueller–Hinton agar. Before inoculation, the swab stick was dipped into bacterial suspension with visually equivalent turbidity to 0.5 McFarland standards. Antibiotic discs (Himedia, India) tested included penicillin G (10 μg), vancomycin (30 μg), erythromycin (15 μg), chloramphenicol (30 μg), co-trimoxazole (25 μg), rifampicin (30 μg), clindamycin (2 μg), amoxicillin-clavulanic acid (20/10 μg), tetracycline (30 μg), ciprofloxacin (5 μg), and cefoxitin (30 μg). The zones of inhibition for each antimicrobial agent were measured and interpreted as resistant, intermediate, or susceptible according to local interpretation rules used in the hospitals of the Gaza strip, which are derived from the CLSI guidelines when available from the technical data sheets of Himedia, or correspond to the former inhibition zone diameter but are still in use in Gaza hospitals to infer antibiotic susceptibility. Thus, co-trimoxazole, vancomycin, and amoxicillin-clavulanic acid were not interpreted using CLSI nor EUCAST guidelines, but using the following zone diameters: R < 10 mm and S ≥ 16 mm for co-trimoxazole; R < 19 mm and S ≥ 20 mm for amoxicillin-clavulanic acid; and R < 17 mm and S ≥ 17 mm for vancomycin. Methicillin resistance was inferred using the zone diameter around cefoxitin following CLSI guidelines [28].

2.5. Statistical Analysis

The results were tabulated and analyzed using the Statistical Package for the Social Sciences (SPSS, version 20). Frequencies, cross-tabulation, and appropriate statistical tests such as the Chi-square test and Fisher’s exact test were performed. A p-value of less than 0.05 was considered significant.

3. Results

3.1. Molecular Analysis

A total of 285 S. aureus isolates were collected from five different hospitals in the Gaza Strip including Al Naser, Al Shifa, Al Aqsa, Europeans, and Nasser hospitals. The number of S. aureus isolates collected from the preceding hospitals was 85, 72, 61, 41, and 26, respectively (Table 2).
The majority of the S. aureus isolates were collected from pus (208/285 [72.9%]), followed by blood (31/285 [10.8%]), sputum (17/285 [5.9%]), urine (14/285 [4.9%]), and other sites of infection such as eye secretion, ear secretion, nasal, skin, umbilical cord, and vaginal discharge (15/285 [5.2%]) (Table 3).
PCR analysis of the 285 clinical S. aureus isolates revealed 200 mecA-positive isolates (70.2% MRSA) while 85 were mecA-negative (29.8% MSSA). The prevalence of MRSA in Al Shifa, Al Naser, Al Aqsa, European, and Nasser hospitals was 76.4%, 70.5%, 65.8%, 69.2%, and 65.6%, respectively. Pvl toxin gene was detected in 85 (29.8%) of all tested isolates. The prevalence of PVL in Al Naser, Al Aqsa, Al Shifa, European, and Nasser hospitals was 32.9%, 31.7%, 29.1%, 26.9, and 26.2%, respectively. The distribution of PVL-positive S. aureus isolates according to the clinical specimens was as follows: pus 70 (33.6%), sputum 6 (35.2%), blood 6 (19.3%), other samples 2 (13.3%), and urine 1 (7.1%), respectively (Table 3). The prevalence of the pvl gene among MRSA and MSSA isolates was 30.5% and 28.2%, respectively.

3.2. Antimicrobial Susceptibility Testing

Disk diffusion antimicrobial susceptibility testing revealed that the least effective antibiotics were penicillin G and amoxicillin-clavulanic acid with resistance rates of 96.1% and 73.6%, respectively (Table 4). The most effective antibiotics were rifampicin, vancomycin, and clindamycin, with susceptibility rates of 91.2%, 88.7%, and 84.6%, respectively. Nearly half of the isolates were resistant to erythromycin (47.7%).
When considering PVL+ isolates, PVL+ MRSA isolates were highly resistant to penicillin G and amoxicillin-clavulanic acid (95% and 83.5%, respectively) but have a low prevalence of resistance to rifampicin, clindamycin, chloramphenicol, and vancomycin (Table 5). PVL+ MSSA isolates have a low prevalence of resistance to amoxicillin-clavulanic acid, vancomycin, co-trimoxazole, rifampicin, and ciprofloxacin in comparison with PVL+ MRSA (Table 5).
The prevalence of MDR, e.g., resistance to at least three families of antibiotics, among S. aureus isolates was 66% (188/285). The prevalence of MDR among MRSA and MSSA isolates was 75.5% (151/200) and 43% (37/85), respectively.

4. Discussion

Panton-Valentine Leukocidin (PVL) is a bicomponent pore-forming cytolytic toxin encoded by the lukF/PV and lukS/PV genes. It was thought as one of the major virulence factors contributing to the morbidity and mortality attributed to S. aureus [14,17,27,29] causing skin and soft tissue infections, such as cutaneous abscesses and severe necrotizing pneumonia. However, the role of PVL toxin in determining the severity of MRSA infections has been and still is controversial. Newer pieces of evidence showed that the presence of pvl genes is neither the primary cause nor the determinant of MRSA infection severity [30,31,32]. Other studies have found that PVL-positive isolates have a high proclivity for invasive infections, but the presence of pvl genes is not the main determinant of MRSA infection severity nor invasivity [33,34]. As a result, it is important to investigate the prevalence of the PVL marker among MRSA isolates, which are a major health concern due to their multidrug resistance [35,36].
In this study, MRSA accounted for 70.2% (n = 200) of the isolates tested by PCR for the mecA gene and 69.1% (n = 197) according to cefoxitin sensitivity testing. This discrepancy may be due to the fact that molecular testing is more sensitive and specific for the diagnosis of MRSA. So, we suggest that molecular approaches should be favored. Moreover, one limitation of this study is that only mecA genes were thought of and that even though rare, future evaluations need to include the mecC gene. The prevalence in our study was higher than that reported by previous studies conducted in Gaza and the West Bank (56.3%, 29%, and 45%, respectively) except for one that reported a slightly higher prevalence (82.3%), which could be explained by the phenotypic detection method used (oxacillin discs) which is known to be less specific than molecular testing [20,21,22,23,37]. Our results are comparable to those reported in Jordan, Egypt, and Cyprus, where more than 50% of the invasive S. aureus isolates were methicillin-resistant [38]. Tabaja et al. reported that the available data suggest a high burden of MRSA in Arab countries of the Middle East and North Africa (MENA) [39]. The prevalence of MRSA (76.3%) in Al Shifa hospital, which is considered the major referral hospital in the Gaza Strip, was higher than that reported from the same hospital by Al Laham et al. (56.3%) in 2015 [20]. Our results were consistent with those reported in Al-Karak hospital and Prince Ali hospital in Jordan (77.5%) [40]. In a recent study in Egypt, a high prevalence of MRSA isolates was identified (138/170, 81.2%) with 79% of isolates (109/138, 79%) being MDR-MRSA [41].
The frequency of PVL-harboring isolates (PVL+) in our study was 29.8%, which is lower than the 40% reported by Al Laham et al. [20]. The highest rate of PVL among hospitals in the Gaza Strip was found in Al Naser and Al Aqsa hospitals (32.9% and 31.7% respectively). In comparison with previous studies that were conducted in Palestine, our results are consistent with those of two hospitals from the West Bank and East Jerusalem [23] (29.5%) but higher than those of Rafidia and Thabet hospitals (West Bank) [37] and from healthy children throughout the Gaza Strip [21] (14.3% and 8.5%, respectively). These differences in PVL prevalence could be a reflection of the different dominant MRSA clones circulating in these regions that may or may not harbor pvl genetic determinants.
Many studies from the Arab countries of the Middle East investigated the molecular epidemiology of clinical S. aureus including detection of the pvl gene. In Saudi Arabia and Alexandria, Egypt, pvl prevalence (48.7% and 40%, respectively) was higher than our findings (29.8%) [42,43]. Meanwhile, a recent study from Kuwait hospitals showed only 21.6% pvl-positive S. aureus isolates [44] and, surprisingly, a study conducted in Oman has revealed the dominance of a pvl-negative clone (ST6-IV/t304) [45].
Finally, our results are in line with a study in Greece that reported a frequency of 27% of PVL genes among MRSA [46], while Omuse et al. from Kenya [47] reported higher rates (42.3%) and Shariati et al. [48] from Iran reported only 10.7%. Subarna Roy et al. from India, have reported an overall 62.85% of PVL prevalence among MRSA and MSSA (MRSA: 85.1% and MSSA: 48.8%) [49]. Other parts of the world reported a lower prevalence of PVL (5% in France, 4.9% in the UK, 8.1% in Saudi Arabia, and 14.3% in Bangladesh [17,50,51,52]), indicating that the prevalence of PVL varies greatly between geographical locations and populations.
In our study, PVL was detected in 30.5% (61/200) of MRSA isolates and in 28.2% (24/85) of MSSA isolates. Our results showed no significant difference between MRSA and MSSA populations in terms of PVL carriage. In Nepal, Algeria, Bangladesh, Greece, and Romania, the prevalence rates of the pvl gene among MSSA were 26%, 16.4%, 27.3%, 12%, and 14%, respectively [46,50,53,54,55]. In Iran, Shariati et al. [48] reported PVL carriage in 18.8% of MRSA and only 3% of MSSA, which is in line with other studies that reported higher prevalence in MRSA isolates than MSSA [1,56,57,58]. However, this is not a general rule, as Alli et al. in Nigeria reported a higher prevalence of the pvl gene in MSSA (53.3%) than in MRSA isolates (9.1%) [59]. This is also consistent with Azar et al., who showed that the prevalence of the pvl gene in MRSA strains was 7.23%, while that in MSSA was 33.3% [60].
PVL is associated with increased virulence of certain S. aureus strains and is the cause of necrotic lesions affecting the skin and mucosa that are extremely difficult to treat, such as necrotic hemorrhagic pneumonia. As a result, early detection of the pvl gene in S. aureus may be critical for treating cases and assessing treatment outcomes.
MRSA was found in 72.2% (150/208 isolates) of S. aureus from pus. The majority of our PVL-positive isolates were isolated from pus and blood samples (72% and 64%, respectively).
S. aureus has a positive relationship with skin and soft tissue infections (SSTIs); in fact, most investigations have found that the frequency of the PVL gene is higher in pus specimens collected from SSTIs compared to blood, urine, or sputum samples [51]. In this study, the prevalence of the pvl gene among sputum, blood, and urine isolates was 60%, 30%, and 11%, respectively.
Kamarehei, et al. [61] reported in Iran that the majority of PVL-carriage isolates (30.4%) were found in wound specimens, and 27.6% of urine specimens were PVL positive, which could play a role in virulence. Singh-Moodley et al. [62] characterized MRSA isolates from blood cultures in South Africa from 2013 to 2016, reporting a PVL positivity rate of 25%, which was lower than the rate in our study.
Our results showed that the least effective antibiotics were penicillin G and amoxicillin-clavulanic acid. Their resistance rate was 96.1% and 73.6%. Demir et al. from Turkey [63] reported a higher rate of sensitivity for amoxicillin-clavulanic acid (53.6%) than our study (26.3%). The resistance rate of PVL-producing MRSA and MSSA strains against penicillin G was 95%. These results are comparable to those of Al Laham et al. [20] in Palestine and Bazzi et al. in Dhahran, Saudi Arabia, which reported 98.9% and 88.75%, resistance, respectively [64].
Surprisingly, only 84.3% of MRSA isolates were susceptible to vancomycin. This result is consistent with that of Islam et al. who reported a susceptibility rate of 86%, but different from other studies in the Gaza Strip and West Bank that reported 100% susceptibility to vancomycin [20,21,23]. Moreover, this discrepancy may be due to visual MacFarland determination because we did not use a nephelometer to determine the 0.5 MacFarland, or it was a reading of one or two millimeters above the CLSI breakpoints.
This implies that vancomycin remains an effective treatment option and is considered a last-resort antibiotic for severe MRSA and other resistant Gram-positive infections [65,66,67,68,69]. The sensitivity rate of MRSA isolates against clindamycin was 88%. Clindamycin has been recommended for the treatment of cutaneous infections related to S. aureus [63].

5. Conclusions

In comparison to previously published results from the Gaza Strip, our study highlights the fact that the rate of multidrug-resistant MRSA among the population is increasing in Palestine as 70.2% of our S. aureus (which were MRSA) isolates were MDR.
Vancomycin, erythromycin, and clindamycin are common examples of antibiotics used for the treatment of infections caused by Gram-positive bacteria, and the susceptibility of the S. aureus clinical isolates in our study to these antimicrobial agents demonstrated that these antibiotics are still effective for the treatment of infections caused by these pathogens.
We reported that 29.8% of MRSA isolates from hospitalized patients from five different hospitals in the Gaza Strip were PVL positive. As PVL is a pathogenicity marker, these PVL-positive isolates are likely more virulent and must be closely monitored and treated.
Thus, given the high prevalence of MRSA, it is critical to screen clinical samples for mecA, but also for pvl genes to properly guide therapy. In addition, continued surveillance and characterization of MRSA isolates in Gaza Strip hospitals are critical for preventing the spread of virulent nosocomial infections and implementing enhanced infection control strategies.

Author Contributions

Conceptualization, N.A.E.A. and N.A.A.L.; validation, N.A.E.A., T.N. and N.A.A.L.; formal analysis, N.A.E.A. and N.A.A.L.; investigation, N.A.E.A. and N.A.A.L.; writing—original draft preparation, N.A.E.A., T.N. and N.A.A.L.; writing—review and editing, N.A.E.A., T.N. and N.A.A.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Ethics Committee and has approval number PHRC/HC/227/17. All ethical considerations and guidelines relating to the collection of the bacterial isolates of S. aureus from different hospitals in the Gaza Strip were followed. The study was approved by the Department of human resources and Development in the Ministry of Health—Gaza.

Informed Consent Statement

The study includes Clinical isolates from the patients in the hospital and agreemnt has been taken from the department of human resources and development in the Ministry of Health. In addition Ehthical approval has been take from Helsinki Committee and has approval number PHRC/HC/227/17.

Data Availability Statement

All data generated or analyzed during this study were included in this article.

Acknowledgments

We are grateful to Emad El-Sheikh and Mohammed Taha for their valuable assistance in different aspects of this work.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Boyle-Vavra, S.; Daum, R.S. Community-acquired methicillin-resistant Staphylococcus aureus: The role of Panton-Valentine leukocidin. Lab. Investig. 2007, 87, 3–9. [Google Scholar] [CrossRef]
  2. Breurec, S.; Fall, C.; Pouillot, R.; Boisier, P.; Brisse, S.; Diene-Sarr, F.; Djibo, S.; Etienne, J.; Fonkoua, M.C.; Perrier-Gros-Claude, J.D.; et al. Epidemiology of methicillin-susceptible Staphylococcus aureus lineages in five major African towns: High prevalence of Panton-Valentine leukocidin genes. Clin. Microbiol. Infect. 2011, 17, 633–639. [Google Scholar] [CrossRef] [PubMed]
  3. Darboe, S.; Dobreniecki, S.; Jarju, S.; Jallow, M.; Mohammed, N.I.; Wathuo, M.; Ceesay, B.; Tweed, S.; Basu Roy, R.; Okomo, U.; et al. Prevalence of Panton-Valentine Leukocidin (PVL) and Antimicrobial Resistance in Community-Acquired Clinical Staphylococcus aureus in an Urban Gambian Hospital: A 11-Year Period Retrospective Pilot Study. Front. Cell Infect. Microbiol. 2019, 9, 170. [Google Scholar] [CrossRef]
  4. Özekinci, T.; Dal, T.; Yanık, K.; Özcan, N.; Can, Ş.; Tekin, A.; Yıldırım, H.; Kandemir, İ. Panton-Valentine leukocidin in community and hospital-acquired Staphylococcus aureus strains. J. Biotechnol. Biotechnol. Equip. 2014, 28, 1089–1094. [Google Scholar] [CrossRef]
  5. Eed, E.M.; Ghonaim, M.M.; Hussein, Y.M.; Saber, T.M.; Khalifa, A.S. Phenotypic and molecular characterization of HA-MRSA in Taif hospitals, Saudi Arabia. J. Infect. Dev. Ctries. 2015, 9, 298–303. [Google Scholar] [CrossRef]
  6. Hartman, B.; Tomasz, A. Altered penicillin-binding proteins in methicillin-resistant strains of Staphylococcus aureus. Antimicrob. Agents Chemother. 1981, 19, 726–735. [Google Scholar] [CrossRef] [PubMed]
  7. Sila, J.; Sauer, P.; Kolar, M. Comparison of the prevalence of genes coding for enterotoxins, exfoliatins, panton-valentine leukocidin and tsst-1 between methicillin-resistant and methicillin-susceptible isolates of Staphylococcus aureus at the university hospital in Olomouc. Biomed. Pap. 2009, 153, 215–218. [Google Scholar] [CrossRef]
  8. Neela, V.; Ehsanollah, G.R.; Zamberi, S.; Van Belkum, A.; Mariana, N.S. Prevalence of Panton-Valentine leukocidin genes among carriage and invasive Staphylococcus aureus isolates in Malaysia. Int. J. Infect. Dis. 2009, 13, e131–e132. [Google Scholar] [CrossRef] [PubMed]
  9. Prévost, G.; Cribier, B.; Couppié, P.; Petiau, P.; Supersac, G.; Finck-Barbançon, V.; Monteil, H.; Piemont, Y. Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect. Immun. 1995, 63, 4121–4129. [Google Scholar] [CrossRef] [PubMed]
  10. Nhan, T.X.; Leclercq, R.; Cattoir, V. Prevalence of toxin genes in consecutive clinical isolates of Staphylococcus aureus and clinical impact. Eur. J. Clin. Microbiol. Infect. Dis. 2011, 30, 719–725. [Google Scholar] [CrossRef]
  11. Lopez-Aguilar, C.; Perez-Roth, E.; Moreno, A.; Duran, M.C.; Casanova, C.; Aguirre-Jaime, A.; Mendez-Alvarez, S. Association between the presence of the Panton-Valentine leukocidin-encoding gene and a lower rate of survival among hospitalized pulmonary patients with staphylococcal disease. J. Clin. Microbiol. 2007, 45, 274–276. [Google Scholar] [CrossRef]
  12. Monecke, S.; Coombs, G.; Shore, A.C.; Coleman, D.C.; Akpaka, P.; Borg, M.; Chow, H.; Ip, M.; Jatzwauk, L.; Jonas, D.; et al. A field guide to pandemic, epidemic, and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS ONE 2011, 6, e17936. [Google Scholar] [CrossRef]
  13. Chambers, H.F. Community-associated MRSA—Resistance and virulence converge. N. Engl. J. Med. 2005, 352, 1485–1487. [Google Scholar] [CrossRef] [PubMed]
  14. Gillet, Y.; Issartel, B.; Vanhems, P.; Fournet, J.C.; Lina, G.; Bes, M.; Vandenesch, F.; Piémont, Y.; Brousse, N.; Floret, D.; et al. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 2002, 359, 753–759. [Google Scholar] [CrossRef]
  15. Chiu, Y.K.; Lo, W.T.; Wang, C.C. Risk factors and molecular analysis of Panton-Valentine leukocidin-positive methicillin-susceptible Staphylococcus aureus colonization and infection in children. J. Microbiol. Immunol. Infect. 2012, 45, 208–213. [Google Scholar] [CrossRef]
  16. Gijón, M.; Bellusci, M.; Petraitiene, B.; Noguera-Julian, A.; Zilinskaite, V.; Sanchez Moreno, P.; Saavedra-Lozano, J.; Glikman, D.; Daskalaki, M.; Kaiser-Labusch, P.; et al. Factors associated with severity in invasive community-acquired Staphylococcus aureus infections in children: A prospective European multicentre study. Clin. Microbiol. Infect. 2016, 22, e641–e646. [Google Scholar] [CrossRef]
  17. Lina, G.; Piémont, Y.; Godail-Gamot, F.; Bes, M.; Peter, M.O.; Gauduchon, V.; Vandenesch, F.; Etienne, J. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis. 1999, 29, 1128–1132. [Google Scholar] [CrossRef]
  18. Hu, Q.; Cheng, H.; Yuan, W.; Zeng, F.; Shang, W.; Tang, D.; Xue, W.; Fu, J.; Zhou, R.; Zhu, J.; et al. Panton-Valentine leukocidin (PVL)-positive health care-associated methicillin-resistant Staphylococcus aureus isolates are associated with skin and soft tissue infections and colonized mainly by infective PVL-encoding bacteriophages. J. Clin. Microbiol. 2015, 53, 67–72. [Google Scholar] [CrossRef]
  19. Adwan, G.; Abu Jaber, A. Frequency and molecular characterization of β-lactamases producing Escherichia coli isolated from North of Palestine. Br. Microbiol. Res. J. 2016, 11, 1–13. [Google Scholar] [CrossRef]
  20. Al Laham, N.; Mediavilla, J.R.; Chen, L.; Abdelateef, N.; Elamreen, F.A.; Ginocchio, C.C.; Pierard, D.; Becker, K.; Kreiswirth, B.N. MRSA clonal complex 22 strains harboring toxic shock syndrome toxin (TSST-1) are endemic in the primary hospital in Gaza, Palestine. PLoS ONE 2015, 10, e0120008. [Google Scholar] [CrossRef]
  21. Biber, A.; Abuelaish, I.; Rahav, G.; Raz, M.; Cohen, L.; Valinsky, L.; Taran, D.; Goral, A.; Elhamdany, A.; Regev-Yochay, G. A typical hospital-acquired methicillin-resistant Staphylococcus aureus clone is widespread in the community in the Gaza strip. PLoS ONE 2012, 7, e42864. [Google Scholar] [CrossRef]
  22. El Aila, N.A.; Al Laham, N.A.; Ayesh, B.M. Nasal carriage of methicillin resistant Staphylococcus aureus among health care workers at Al Shifa hospital in Gaza Strip. BMC Infect. Dis. 2017, 17, 28. [Google Scholar] [CrossRef]
  23. Hadyeh, E.; Azmi, K.; Seir, R.A.; Abdellatief, I.; Abdeen, Z. Molecular Characterization of Methicillin Resistant Staphylococcus aureus in West Bank-Palestine. Front. Public Health 2019, 7, 130. [Google Scholar] [CrossRef]
  24. Wikipedia Contributors. Demographics of the Palestinian Territories. Wikipedia, The Free Encyclopedia. 2022. Available online: http://en.wikipedia.org/wiki/Demographics_of_the_Palestinian_territories (accessed on 7 November 2022).
  25. Kateete, D.P.; Kimani, C.N.; Katabazi, F.A.; Okeng Okee, M.S.; Nanteza, A.; Joloba, M.L.; Najjuka, F.C. Identification of Staphylococcus aureus: DNase and Mannitol salt agar improve the efficiency of the tube coagulase test. Ann. Clin. Microbiol. Antimicrob. 2010, 9, 23–29. [Google Scholar] [CrossRef]
  26. El Aila, N.A.; Tency, I.; Claeys, G.; Saerens, B.; De Backer, E.; Temmerman, M.; Verhelst, R.; Vaneechoutte, M. Genotyping of Streptococcus agalactiae (group B streptococci) isolated from vaginal and rectal swabs of women at 35–37 weeks of pregnancy. BMC Infect. Dis. 2009, 9, 153. [Google Scholar] [CrossRef] [PubMed]
  27. Valle, D.L., Jr.; Paclibare, P.A.; Cabrera, E.C.; Rivera, W.L. Molecular and phenotypic characterization of methicillin-resistant Staphylococcus aureus isolates from a tertiary hospital in the Philippines. Trop. Med. Health 2016, 44, 3. [Google Scholar] [CrossRef]
  28. Performance Standards for Antimicrobial Susceptibility Testing, 26th ed.; Clinical and Laboratory Standard Institute: Wayne, PA, USA, 2021.
  29. Gillet, Y.; Etienne, J.; Lina, G.; Vandenesch, F. Association of necrotizing pneumonia with Panton-Valentine leukocidin-producing Staphylococcus aureus, regardless of methicillin resistance. Clin. Infect. Dis. 2008, 47, 985–986. [Google Scholar] [CrossRef]
  30. Turner, N.A.; Sharma-Kuinkel, B.K.; Maskarinec, S.A.; Eichenberger, E.M.; Shah, P.P.; Carugati, M.; Holland, T.L.; Fowler, V.G., Jr. Methicillin-resistant Staphylococcus aureus: An overview of basic and clinical research. Nat. Rev. Microbiol. 2019, 17, 203–218. [Google Scholar] [CrossRef]
  31. Boakes, E.; Kearns, A.M.; Badiou, C.; Lina, G.; Hill, R.L.; Ellington, M.J. Do differences in Panton-Valentine leukocidin production among international methicillin-resistant Staphylococcus aureus clones affect disease presentation and severity? J. Clin. Microbiol. 2012, 50, 1773–1776. [Google Scholar] [CrossRef] [PubMed]
  32. Tong, A.; Tong, S.Y.C.; Zhang, Y.; Lamlertthon, S.; Sharma-Kuinkel, B.K.; Rude, T.; Ahn, S.H.; Ruffin, F.; Llorens, L.; Tamarana, G.; et al. Panton-Valentine Leukocidin Is Not the Primary Determinant of Outcome for Staphylococcus aureus Skin Infections: Evaluation from the CANVAS Studies. PLoS ONE 2012, 7, e37212. [Google Scholar] [CrossRef]
  33. Shallcross, L.J.; Fragaszy, E.; Johnson, A.M.; Hayward, A.C. The role of the Panton-Valentine leucocidin toxin in staphylococcal disease: A systematic review and meta-analysis. Lancet Infect. Dis. 2013, 13, 43–54. [Google Scholar] [CrossRef] [PubMed]
  34. Wehrhahn, M.C.; Robinson, J.O.; Pearson, J.C.; O’Brien, F.G.; Tan, H.L.; Coombs, G.W.; Pascoe, E.M.; Lee, R.; Salvaris, P.; Salvaris, R.; et al. Clinical and laboratory features of invasive community-onset methicillin-resistant Staphylococcus aureus infection: A prospective case-control study. Eur. J. Clin. Microbiol. Infect. Dis. 2010, 29, 1025–1033. [Google Scholar] [CrossRef] [PubMed]
  35. Dumitrescu, O.; Badiou, C.; Bes, M.; Reverdy, M.E.; Vandenesch, F.; Etienne, J.; Lina, G. Effect of antibiotics, alone and in combination, on Panton-Valentine leukocidin production by a Staphylococcus aureus reference strain. Clin. Microbiol. Infect. 2008, 14, 384–388. [Google Scholar] [CrossRef]
  36. Vandenesch, F.; Naimi, T.; Enright, M.C.; Lina, G.; Nimmo, G.R.; Heffernan, H.; Liassine, N.; Bes, M.; Greenland, T.; Reverdy, M.E.; et al. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: Worldwide emergence. Emerg. Infect. Dis. 2003, 9, 978–984. [Google Scholar] [CrossRef]
  37. Adwan, G.; Shaheen, H.; Adwan, K.; Barakat, A. Molecular characterization of methicillin resistant Staphylococcus aureus isolated from hospitals environments and patients in Northern Palestine. J. Epidemiol. Biostat. Public Health 2015, 12, e11183. [Google Scholar] [CrossRef]
  38. Borg, M.A.; de Kraker, M.; Scicluna, E.; van de Sande-Bruinsma, N.; Tiemersma, E.; Monen, J.; Grundmann, H. Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in invasive isolates from southern and eastern Mediterranean countries. J. Antimicrob. Chemother. 2007, 60, 1310–1315. [Google Scholar] [CrossRef]
  39. Tabaja, H.; Hindy, J.R.; Kanj, S.S. Epidemiology of Methicillin-Resistant Staphylococcus aureus in Arab Countries of the Middle East and North African (MENA) Region. Med. J. Hematol. Infect. Dis. 2021, 13, 2021050. [Google Scholar] [CrossRef]
  40. Jarajreh, D.; Aqel, A.; Alzoubi, H.; Al-Zereini, W. Prevalence of inducible clindamycin resistance in methicillin-resistant Staphylococcus aureus: The first study in Jordan. J. Infect. Dev. Count. 2017, 11, 350–354. [Google Scholar] [CrossRef] [PubMed]
  41. Alfeky, A.E.; Tawfick, M.M.; Ashour, M.S.; El-Moghazy, A.A. High Prevalence of Multi-drug Resistant Methicillin-Resistant Staphylococcus aureus in Tertiary Egyptian Hospitals. J. Infect. Dev. Count. 2022, 16, 795–806. [Google Scholar] [CrossRef]
  42. Senok, A.; Ehricht, R.; Monecke, S.; Al-Saedan, R.; Somily, A. Molecular characterization of methicillin resistant Staphylococcus aureus in nosocomial infections in a tertiary care facility: Emergence of new clonal complexes in Saudi Arabia. New Microbes New Infect. 2016, 14, 13–18. [Google Scholar] [CrossRef]
  43. Monecke, S.; Bedewy, A.K.; Müller, E.; Braun, S.D.; Diezel, C.; Elsheredy, A.; Kader, O.; Reinicke, M.; Ghazal, A.; Rezk, S.; et al. Characterization of Methicillin Resistant Staphylococcus aureus from Alexandria, Egypt. Antibiotics 2023, 12, 78. [Google Scholar] [CrossRef] [PubMed]
  44. Udo, E.E.; Boswihi, S.S.; Al-Sweih, N. High prevalence of toxic shock syndrome toxin-producing epidemic methicillin-resistant Staphylococcus aureus 15 (EMRSA-15) strains in Kuwait hospitals. New Microbes New Infect. 2016, 12, 24–30. [Google Scholar] [CrossRef]
  45. Udo, E.E.; Al-Lawati, B.A.-H.; Al-Muharmi, Z.; Thukral, S.S. Genotyping of methicillin-resistant Staphylococcus aureus in the Sultan Qaboos University Hospital, Oman reveals the dominance of Panton–Valentine leucocidin-negative ST6-IV/t304 clone. New Microbe New Infect. 2014, 2, 100–105. [Google Scholar] [CrossRef] [PubMed]
  46. Chini, V.; Petinaki, E.; Foka, A.; Paratiras, S.; Dimitracopoulos, G.; Spiliopoulou, I. Spread of Staphylococcus aureus clinical isolates carrying Panton-Valentine leukocidin genes during a 3-year period in Greece. Clin. Microbiol. Infect. 2006, 12, 29–34. [Google Scholar] [CrossRef]
  47. Omuse, G.; Shivachi, P.; Kariuki, S.; Revathi, G. Prevalence of panton valentine leukocidin in carriage and infective strains of Staphylococcus aureus at a referral hospital in Kenya. Open J. Med. Microbiol. 2013, 3, 5–11. [Google Scholar] [CrossRef]
  48. Shariati, L.; Validi, M.; Hasheminia, A.M.; Ghasemikhah, R.; Kianpour, F.; Karimi, A.; Nafisi, M.R.; Tabatabaiefar, M.A. Staphylococcus aureus Isolates Carrying Panton-Valentine Leucocidin Genes: Their Frequency, Antimicrobial Patterns, and Association With Infectious Disease in Shahrekord City, Southwest Iran. Jundishapur J. Microbiol. 2016, 9, e28291. [Google Scholar] [CrossRef]
  49. Kaur, H.; Purwar, S.; Saini, A.; Kaur, H.; Karadesai, S.; Kholkute, S.; Roy, S.J.J. Status of methicillin-resistant Staphylococcus aureus infections and evaluation of PVL producing strains in Belgaum, South India. J. Krishna Inst. Med. Sci. Univ. 2012, 1, 43–51. [Google Scholar]
  50. Afroz, S.; Kobayashi, N.; Nagashima, S.; Alam, M.M.; Hossain, A.B.; Rahman, M.A.; Islam, M.R.; Lutfor, A.B.; Muazzam, N.; Khan, M.A.; et al. Genetic characterization of Staphylococcus aureus isolates carrying Panton-Valentine leukocidin genes in Bangladesh. Jpn. J. Infect. Dis. 2008, 61, 393–396. [Google Scholar] [CrossRef] [PubMed]
  51. Holmes, A.; Ganner, M.; McGuane, S.; Pitt, T.L.; Cookson, B.D.; Kearns, A.M. Staphylococcus aureus isolates carrying Panton-Valentine leucocidin genes in England and Wales: Frequency, characterization, and association with clinical disease. J. Clin. Microbiol. 2005, 43, 2384–2390. [Google Scholar] [CrossRef]
  52. Moussa, I.; Hessan, A. Rapid detection of community acquired-methicillin resistance Staphylococcus aureus recovered from King Saudi Arabia. Afr. J. Microbiol. Res. 2010, 4, 2804–2810. [Google Scholar]
  53. Antri, K.; Rouzic, N.; Boubekri, I.; Dauwalder, O.; Beloufa, A.; Ziane, H.; Djennane, F.; Neggazi, M.; Benhabyles, B. High prevalence of community-and hospital-acquired infections of methicillin-resistant Staphylococcus aureus containing Panton-Valentine leukocidin gene in Algiers. J. Pathol. Biol. 2009, 58, e15–e20. [Google Scholar] [CrossRef]
  54. Monecke, S.; Müller, E.; Dorneanu, O.S.; Vremeră, T.; Ehricht, R. Molecular typing of MRSA and of clinical Staphylococcus aureus isolates from Iaşi, Romania. PLoS ONE 2014, 9, e97833. [Google Scholar] [CrossRef] [PubMed]
  55. Shrestha, B.; Singh, W.; Raj, V.S.; Pokhrel, B.M.; Mohapatra, T.M. High prevalence of Panton-Valentine leukocidin (PVL) genes in nosocomial-acquired Staphylococcus aureus isolated from tertiary care hospitals in Nepal. BioMed Res. Internet 2014, 2014, 790350. [Google Scholar]
  56. Brown, M.L.; O’Hara, F.P.; Close, N.M.; Mera, R.M.; Miller, L.A.; Suaya, J.A.; Amrine-Madsen, H. Prevalence and sequence variation of panton-valentine leukocidin in methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains in the United States. J. Clin. Microbiol. 2012, 50, 86–90. [Google Scholar] [CrossRef] [PubMed]
  57. Jiménez, J.N.; Ocampo, A.M.; Vanegas, J.M.; Rodríguez, E.A.; Garcés, C.G.; Patiño, L.A.; Ospina, S.; Corre, A.M.M. Characterisation of virulence genes in methicillin susceptible and resistant Staphylococcus aureus isolates from a paediatric population in a university hospital of Medellín, Colombia. Mem. Inst. Oswaldo Cruz 2011, 106, 980–985. [Google Scholar] [CrossRef]
  58. Vourli, S.; Vagiakou, H.; Ganteris, G.; Orfanidou, M.; Polemis, M.; Vatopoulos, A.; Malamou-Ladas, H. High rates of community-acquired, Panton-Valentine leukocidin (PVL)-positive methicillin-resistant S. aureus (MRSA) infections in adult outpatients in Greece. Euro Surveill. 2009, 14, 19089. [Google Scholar]
  59. Alli, O.; Ogbolu, D.O.; Shittu, A.O.; Okorie, A.N.; Akinola, J.O.; Daniel, J.B. Association of virulence genes with mecA gene in Staphylococcus aureus isolates from Tertiary Hospitals in Nigeria. Indian J. Pathol. Microbiol. 2015, 58, 464. [Google Scholar] [CrossRef]
  60. Khosravi, A.D.; Hoveizavi, H.; Farshadzadeh, Z. The prevalence of genes encoding leukocidins in Staphylococcus aureus strains resistant and sensitive to methicillin isolated from burn patients in Taleghani Hospital, Ahvaz, Iran. Burns 2012, 38, 247–251. [Google Scholar] [CrossRef]
  61. Kamarehei, F.; Ghaemi, E.A.; Dadgar, T. Prevalence of enterotoxin A and B genes in Staphylococcus aureus isolated from clinical samples and healthy carriers in Gorgan City, North of Iran. Indian J. Pathol. Microbiol. 2013, 56, 265–268. [Google Scholar]
  62. Singh-Moodley, A.; Strasheim, W.; Mogokotleng, R.; Ismail, H.; Perovic, O. Unconventional SCCmec types and low prevalence of the Panton-Valentine Leukocidin exotoxin in South African blood culture Staphylococcus aureus surveillance isolates, 2013-2016. PLoS ONE 2019, 14, e0225726. [Google Scholar] [CrossRef]
  63. Demir, T.; Coplu, N.; Bayrak, H.; Turan, M.; Buyukguclu, T.; Aksu, N.; Eksioglu, M.; Yalcin, B.; Atakan, N.; Kilic, S.; et al. Panton-Valentine leucocidin gene carriage among Staphylococcus aureus strains recovered from skin and soft tissue infections in Turkey. J. Antimicrob. Chemother. 2012, 67, 837–840. [Google Scholar] [CrossRef] [PubMed]
  64. Bazzi, A.M.; Rabaan, A.A.; Fawarah, M.M.; Al-Tawfiq, J.A. Prevalence of Panton-Valentine leukocidin-positive methicillin-susceptible Staphylococcus aureus infections in a Saudi Arabian hospital. J. Infect. Public Health 2015, 8, 364–368. [Google Scholar] [CrossRef] [PubMed]
  65. Ghasemian, R.; Najafi, N.; Makhlough, A.; Khademloo, M. Frequency of nasal carriage of Staphylococcus aureus and its antimicrobial resistance pattern in patients on hemodialysis. Iran. J. Kidney Dis. 2010, 4, 218–222. [Google Scholar] [PubMed]
  66. Hafeez, R.; Chughtai, A.; Aslam, M. Prevalence and antimicrobial susceptibility of methicillin resistant Staphylococcus aureus (MRSA). J. Int. Pathol. 2004, 2, 10–15. [Google Scholar]
  67. Orji, O.; Olayinka, B.; Afolabi, B.; Ejikeugwu, C. Molecular detection of panton-valentine leukocidin (PVL) toxins in clinical isolates of Staphylococcus aureus from Maitama district hospital, Abuja, Nigeria. J. Med. Microbiol. Diagn. 2016, 5, 240. [Google Scholar]
  68. Taj, Y.; Abdullah, F.E.; Kazmi, S.U. Current pattern of antibiotic resistance in Staphylococcus aureus clinical isolates and the emergence of vancomycin resistance. J. Coll. Phys. Surg. 2010, 20, 728–732. [Google Scholar]
  69. Harrison, E.M.; Paterson, J.K.; Holden, M.T.; Xiaoliang, B.; Ba, X.; Rolo, J.; Morgan, F.J.; Holmes, M.A. A novel hybrid SCCmec-mecC region in Staphylococcus sciuri. J. Antimicrob. Chemother. 2014, 69, 911–918. [Google Scholar] [CrossRef]
Table
Table 1. PCR primers used in this study.
Table 1. PCR primers used in this study.
PrimersGene TargetedSequenceProduct Size (bp)
Staph756F16SRNA5-AACTCTGTTATTAGGGAAGAACA-3
Staph750R16SRNA5-CCACCTTCCTCCGGTTTGTCACC-3756
Leuk-PV-1lukS/F5-ATCATTAGGTAAAATGTCTGGACATGATCCA-3
Leuk-PV-2lukS/F5-GCATCAAGTGTATTGGATAGCAAAA GC-3433
Mec-A1mecA5-GTAGAAATGACTGAACGTCCGATAA-3
Mec-A2mecA5-CCAATTCCACATTGT TTCGGTCTAA-3310
Table
Table 2. Prevalence of mecA and pvl genes according to the hospitals in the Gaza Strip.
Table 2. Prevalence of mecA and pvl genes according to the hospitals in the Gaza Strip.
MRSAMSSAPVLMRSA
PVL+		MRSA
PVL−		MSSA
PVL+		MSSA
PVL−
Al Shifa (72)55
(76.3%)		17
(23.6%)		21
(29.1%)		15
(20.8%)		40
(55.5%)		6
(8.3%)		11
(15.2%)
Al Nasser (85)60
(70.5%)		25
(29.4%)		28
(32.9%)		21
(24.7%)		39
(45.8%)		7
(8.2%)		18
(21.1%)
Al Aqsa (41)27
(65.8%)		14
(34.1%)		13
(31.7%)		8
(19.5%)		19
(46.3%)		5
(12.1%)		9
(21.9%)
European (26)18
(69.2%)		8
(30.8%)		7
(26.9%)		6
(23%)		12
(46.1%)		1
(3.8%)		7
(26.9%)
Naser (61)40
(65.6%)		21
(52.5%)		16
(26.2%)		11
(18%)		29
(47.5%)		5
(8.1%)		16
(26.2%)
Total (285)200
(70.1%)		85
(29.8%)		85
(29.8%)		61
(21.4%)		139
(48.7%)		24
(8.4%)		61
(21.4%)
Table
Table 3. Prevalence of mecA and pvl genes according to the sample type.
Table 3. Prevalence of mecA and pvl genes according to the sample type.
MRSAMSSAPVLMRSA/PVL+MRSA/PVL−MSSA/PVL+MSSA/PVL−Total/Sample Type
Blood201164162931
Sputum 1076462517
Pus 150587051991939208
Urine 951180514
Others11421101315
Total2008585611392461285
Table
Table 4. Antibiotic Susceptibility profile of S. aureus.
Table 4. Antibiotic Susceptibility profile of S. aureus.
R $S $I $
No.%No.%No.%
Penicillin G27496.1113.900
Amoxicillin/
Clavulanic Acid *		21073.67526.300
Cefoxitin19869.58730.500
Erythromycin13647.713246.3176
Co-trimoxazole *9232.318564.982.8
Tetracycline7927.220672.300
Ciprofloxacin7526.219367.7176
Chloramphenicol5218.222980.441.4
Vancomycin *3211.225388.700
Clindamycin3110.924184.6134.5
Rifampicin238.126091.220.7
$ Legend: R: Resistant. S: sensitive, I: Intermediate. * For these antibiotics, antibiotic susceptibility was not interpreted following CLSI nor EUCAST guidelines but using former CLSI inhibition diameters that are still in use in Gaza hospitals. Thus, the following zone diameters were used: R < 10 mm and S ≥ 16 mm for co-trimoxazole; R < 19 mm and S ≥ 20 mm for amoxicillin-clavulanic acid; and R < 17 mm and S ≥ 17 mm for vancomycin.
Table
Table 5. Antibiotic resistance profile of S. aureus according to mecA and pvl positivity.
Table 5. Antibiotic resistance profile of S. aureus according to mecA and pvl positivity.
MRSA
(n = 200)		MSSA
(n = 85)		MRSA/PVL+
(n = 61)		MRSA/PVL−
(n = 139)		MSSA/
PVL+
(n = 24)		MSSA/
PVL−
(n = 61)
Penicillin G197
(98.5%)		81
(95.2%)		58
(95%)		139
(100%)		23
(95.5%)		58
(95%)
Amoxicillin/
Clavulanic Acid *		160
(80%)		53
(62%)		51
(83.6%)		108
(77.6%)		13
(54.5%)		40
(65.5%)
Cefoxitin197
(98.5%)		80
(32.9%)		59
(96.7%)		139
(100%)		23
(95.5%)		57
(93.4%)
Erythromycin95
(47.5%)		39
(45.8%)		29
(47.5%)		66
(47.5%)		10
(41.6%)		29
(47.5%)
Co-trimoxazole *73
(36.5%)		17
(20%)		20
(32.7%)		53
(38.1%)		1
(4.1%)		16
(26.2%)
Tetracycline48
(24%)		18
(21%)		19
(31.1%)		40
(28.7%)		6
(25%)		12
(18.7%)
Ciprofloxacin60
(30%)		15
(17.6%)		17
(27.8%)		38
(27.3%)		1
(4.7%)		13
(21.3%)
Chloramphenicol34
(17%)		18
(21.1%)		8
(13.1%)		26
(18.7%)		5
(20.8%)		13
(21.3%)
Rifampicin21
(10.5%)		2
(2.3%)		5
(8.1%)		16
(11.5%)		1
(4.1%)		1
(1.6%)
Vancomycin *31
(15.5%)		10
(5%)		10
(16.3%)		16
(11.5%)		2
(8.3%)		8
(13%)
Clindamycin24
(12%)		6
(7%)		5
(8.1%)		19
(13.6%)		2
(8.3%)		4
(6.5%)
* For these antibiotics, antibiotic susceptibility was not interpreted following CLSI nor EUCAST guidelines but using former CLSI inhibition diameters that are still in use in Gaza hospitals. Thus, the following zone diameters were used: R < 10 mm and S ≥ 16 mm for co-trimoxazole; R < 19 mm and S ≥ 20 mm for amoxicillin-clavulanic acid; and R < 17 mm and S ≥ 17 mm for vancomycin.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

El Aila, N.A.; Al Laham, N.A.; Naas, T. Prevalence of mecA and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Clinical Isolates from Gaza Strip Hospitals. Microorganisms 2023, 11, 1155. https://doi.org/10.3390/microorganisms11051155

AMA Style

El Aila NA, Al Laham NA, Naas T. Prevalence of mecA and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Clinical Isolates from Gaza Strip Hospitals. Microorganisms. 2023; 11(5):1155. https://doi.org/10.3390/microorganisms11051155

Chicago/Turabian Style

El Aila, Nabil Abdullah, Nahed Ali Al Laham, and Thierry Naas. 2023. "Prevalence of mecA and Panton-Valentine Leukocidin Genes in Staphylococcus aureus Clinical Isolates from Gaza Strip Hospitals" Microorganisms 11, no. 5: 1155. https://doi.org/10.3390/microorganisms11051155

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