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Antimicrob Agents Chemother. Mar 2006; 50(3): 1083–1085.
PMCID: PMC1426459

Detection of Methicillin-Resistant Staphylococcus aureus Strains Resistant to Multiple Antibiotics and Carrying the Panton-Valentine Leukocidin Genes in an Algiers Hospital


Forty-five Panton-Valentine leukocidin (PVL)-positive, methicillin-resistant Staphylococcus aureus strains were isolated in Algeria between 2003 and 2004; 18 isolates were isolated in the community and 27 in a hospital. Five PVL-positive hospital isolates were resistant to multiple antibiotics, including ofloxacin and gentamicin for three isolates.

First identified in the 1960s, methicillin-resistant Staphylococcus aureus (MRSA) was initially considered a nosocomial pathogen. However, in recent years, increasing numbers of MRSA strains have been isolated worldwide from patients with community-acquired infections (1, 5, 7-10, 12, 24, 28). Two main types of MRSA now circulate in the community: (i) hospital-derived strains (H-MRSA) that infect patients with risk factors such as recent hospitalization, surgery, underlying chronic diseases, or immunosuppression and (ii) strains arising de novo in the community (C-MRSA) and infecting patients with no established risk factors. C-MRSA strains tend to be susceptible to more antibiotics than H-MRSA strains, but C-MRSA strains from the United States were reported to be resistant to erythromycin and fluoroquinolones in 2005 (26). C-MRSA strains also harbor specific virulence genes associated with skin and soft-tissue infections, including the Panton-Valentine leukocidin (PVL) genes. Other virulence factors, such as superantigenic toxins, had been detected also in some C-MRSA strains (26, 28). C-MRSA strains have a small methicillin resistance cassette (SCCmec type IV or V), whereas most H-MRSA strains have a larger cassette (SCCmec type I or II) (6, 20, 24, 28).

Epidemiological data on MRSA in Africa are scarce. The prevalence of MRSA was determined in eight African countries between 1996 and 1997 and was relatively high in Nigeria, Kenya, and Cameroon (21 to 30%) and below 10% in Tunisia and Algeria (15). In Algeria, the rate increased to 14% in 2001 (25). PVL-positive C-MRSA strains are thought to circulate in Algeria, based on reports of infections in patients originating from Algeria but generally diagnosed in Europe (10, 17).

Mustapha Pacha hospital is the largest hospital in Algeria, with 1,800 beds. Between 2003 and 2004, 614 S. aureus strains were cultured and identified by the laboratory and 204 (33.2%) were found to be resistant to methicillin. Here we determined the toxin expression and genomic characteristics of 61 randomly selected MRSA strains isolated in this hospital from patients with community-acquired infections (20 cases) or hospital-acquired infections (41 cases).

Species identification was based on colony morphology and microscopic examination and on the results of the coagulase rabbit plasma and Staphyslide agglutination tests (bioMérieux). Antimicrobial susceptibility was determined by the disk diffusion method according to Clinical and Laboratory Standards Institute (formerly the National Committee for Clinical and Laboratory Standards) recommendations (21a). The mecA gene coding for methicillin resistance was detected by PCR as described elsewhere (19). The toxic shock syndrome toxin gene (tst), the PVL genes (lukS-PV and lukF-PV), and accessory gene regulator alleles (agr types 1 to 4) were detected by PCR as previously described (10, 13, 14, 18). Pulsed-field gel electrophoresis of genomic DNA was performed after SmaI digestion as previously described (10), and multilocus sequence typing was performed as described by Enright et al. (11).

The most frequently detected toxin genes were the PVL genes (45/61 isolates, 72%). The PVL genes were harbored by a major clone accounting for 44 of the 45 PVL-positive isolates. This clone had the following characteristics: sequence type 80 (ST80), agr type 3, and SCCmec type IV. The PFGE patterns of these 44 isolates showed more than 80% similarity (Fig. (Fig.1).1). Forty-three isolates (97.6%) were resistant to kanamycin, 38 (86%) were resistant to fusidic acid, 32 (73%) were resistant to tetracycline, 11 (25%) were resistant to erythromycin, 7 (16%) were resistant to ofloxacin, 5 (11.3%) were resistant to clindamycin, 3 (7%) were resistant to gentamicin, 2 (4.5%) were resistant to pristinamycin, 1 (2.3%) was resistant to chloramphenicol, and 1 (2.3%) was resistant to rifampin (Table (Table1).1). Another PVL-positive clone was represented by a single isolate (ST5, agr type 2, SCCmec type IVA). PVL-positive isolates caused 18 (86%) of the 21 community-acquired infections and 27 (67.5%) of the 40 hospital-acquired infections.

FIG. 1.
Dendrogram of Algerian H-MRSA and C-MRSA isolates with genetic characteristics such as ST, agr allele group, toxin gene profile (PVL and tst genes), mecA gene, SCCmec typing, and PFGE patterns. Fragment sizes (in kilobases) of reference strain NCTC8325 ...
Antibiotic resistance profiles of PVL-positive MRSA detected at Mustapha Pacha Hospital

PVL-positive MRSA strains thus appear to be widespread in Mustapha Pacha Hospital, although it is possible that the patients concerned were nasal carriers on admission (23). The high incidence of H-MRSA infection associated with PVL-positive S. aureus strains suggests the occurrence of a hospital outbreak due to this clone. Health care workers can also disseminate MRSA (2, 22, 27). The carriage rate of PVL-positive MRSA in the Algiers community is not known, but a high carriage rate might lead to an increase in hospital infections.

PVL-positive ST80 C-MRSA strains are usually resistant to oxacillin, kanamycin, tetracycline, and fusidic acid (28), and it is particularly worrisome that we detected multidrug-resistant, PVL-positive MRSA causing hospital-acquired infections. Three of our PVL-positive MRSA isolates were resistant to both gentamicin and ofloxacin, drastically restricting treatment options. Two other PVL-positive MRSA isolates were resistant to ofloxacin but susceptible to gentamicin.

Among the C-MRSA isolates, a minor clone (ST37, agr type 3, SCCmec IVA) was detected in two patients and was found to harbor the tst gene. TSST-1-positive C-MRSA strains with an agr type 2 ST5 background have been linked to the neonatal toxic shock-like exanthematous diseases in Japan, while TSST-1-positive C-MRSA strains with an ST5 SCCmec II background have been linked to toxic shock syndrome in Belgium (16).

Five of the 13 PVL- and TSST-1-negative H-MRSA isolates were agr type 1, SCCmec type III, and ST239, ST241, or ST637. These characteristics resemble those of the Brazilian and Hungarian MRSA clones (ST239 and agr type 1). Six H-MRSA isolates were agr type 2, SCCmec type IV or IVA, and ST5, thus resembling the MRSA pediatric clone (2-4). The last two H-MRSA isolates were agr type 3, SCCmec IV, and ST80 or ST635 (a single variant of ST80). Both were PVL negative but were related to the major PVL-positive clone of ST80. As PVL is encoded by phages, these two isolates may have lost the PVL genes (21).

These results show a very high prevalence of PVL-positive MRSA in Mustapha Pacha Hospital in Algiers. These strains were resistant to multiple antibiotics, including gentamicin and ofloxacin. The treatment options in the case of multiple-antibiotic-resistant MRSA strains included cotrimoxazole or pristinamycin for minor infections and glycopeptides for severe infections. Poor infection control procedures in this institution may have enabled community-acquired ST80 MRSA to supplant true hospital-acquired MRSA (ST5, ST239, ST241, and ST637). Local physicians must be informed of the emergence of such highly virulent strains and must also be aware of their implications for empirical treatment.


We thank C. Courtier and C. Gardon for technical assistance and D.Young for editing the manuscript.


1. Adhikari, R. P., G. M. Cook, I. Lamont, S. Lang, H. Heffernan, and J. M. Smith. 2002. Phenotypic and molecular characterization of community occurring, Western Samoan phage pattern methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 50:825-831. [PubMed]
2. Aires de Sousa, M., C. Bartzavali, I. Spiliopoulou, I. S. Sanches, M. I. Crisostomo, and H. de Lencastre. 2003. Two international methicillin-resistant Staphylococcus aureus clones endemic in a university hospital in Patras, Greece. J. Clin. Microbiol. 41:2027-2032. [PMC free article] [PubMed]
3. Aires de Sousa, M., and H. de Lencastre. 2003. Evolution of sporadic isolates of methicillin-resistant Staphylococcus aureus (MRSA) in hospitals and their similarities to isolates of community-acquired MRSA. J. Clin. Microbiol. 41:3806-3815. [PMC free article] [PubMed]
4. Baba, T., F. Takeuchi, M. Kuroda, H. Yuzawa, K. Aoki, A. Oguchi, Y. Nagai, N. Iwama, K. Asano, T. Naimi, H. Kuroda, L. Cui, K. Yamamoto, and K. Hiramatsu. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:1819-1827. [PubMed]
5. Barrett, F. F., R. F. McGehee, Jr., and M. Finland. 1968. Methicillin-resistant Staphylococcus aureus at Boston City Hospital. Bacteriologic and epidemiologic observations. N. Engl. J. Med. 279:441-448. [PubMed]
6. Boyle-Vavra, S., B. Ereshefsky, C. C. Wang, and R. S. Daum. 2005. Successful multiresistant community-associated methicillin-resistant Staphylococcus aureus lineage from Taipei, Taiwan, that carries either the novel staphylococcal chromosome cassette mec (SCCmec) type VT or SCCmec type IV. J. Clin. Microbiol. 43:4719-4730. [PMC free article] [PubMed]
7. Centers for Disease Control and Prevention. 1999. Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus—Minnesota and North Dakota, 1997-1999. JAMA 282:1123-1125. [PubMed]
8. Collignon, P., I. Gosbell, A. Vickery, G. Nimmo, T. Stylianopoulos, and T. Gottlieb. 1998. Community-acquired methicillin-resistant Staphylococcus aureus in Australia. Lancet 352:145-146. [PubMed]
9. Denis, O., A. Deplano, H. De Beenhouwer, M. Hallin, G. Huysmans, M. G. Garrino, Y. Glupczynski, X. Malaviolle, A. Vergison, and M. J. Struelens. 2005. Polyclonal emergence and importation of community-acquired methicillin-resistant Staphylococcus aureus strains harbouring Panton-Valentine leucocidin genes in Belgium. J. Antimicrob. Chemother. 56:1103-1106. [PubMed]
10. Dufour, P., Y. Gillet, M. Bes, G. Lina, F. Vandenesch, D. Floret, J. Etienne, and H. Richet. 2002. Community-acquired methicillin-resistant Staphylococcus aureus infections in France: emergence of a single clone that produces Panton-Valentine leukocidin. Clin. Infect. Dis. 35:819-824. [PubMed]
11. Enright, M. C., N. P. Day, C. E. Davies, S. J. Peacock, and B. G. Spratt. 2000. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38:1008-1015. [PMC free article] [PubMed]
12. Herold, B. C., L. C. Immergluck, M. C. Maranan, D. S. Lauderdale, R. E. Gaskin, S. Boyle-Vavra, C. D. Leitch, and R. S. Daum. 1998. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA 279:593-598. [PubMed]
13. Jarraud, S., C. Mougel, J. Thioulouse, G. Lina, H. Meugnier, F. Forey, X. Nesme, J. Etienne, and F. Vandenesch. 2002. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect. Immun. 70:631-641. [PMC free article] [PubMed]
14. Jarraud, S., M. A. Peyrat, A. Lim, A. Tristan, M. Bes, C. Mougel, J. Etienne, F. Vandenesch, M. Bonneville, and G. Lina. 2001. egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J. Immunol. 166:669-677. [PubMed]
15. Kesah, C., S. Ben Redjeb, T. O. Odugbemi, C. S. Boye, M. Dosso, J. O. Ndinya Achola, S. Koulla-Shiro, M. Benbachir, K. Rahal, and M. Borg. 2003. Prevalence of methicillin-resistant Staphylococcus aureus in eight African hospitals and Malta. Clin. Microbiol. Infect. 9:153-156. [PubMed]
16. Kikuchi, K., N. Takahashi, C. Piao, K. Totsuka, H. Nishida, and T. Uchiyama. 2003. Molecular epidemiology of methicillin-resistant Staphylococcus aureus strains causing neonatal toxic shock syndrome-like exanthematous disease in neonatal and perinatal wards. J. Clin. Microbiol. 41:3001-3006. [PMC free article] [PubMed]
17. Liassine, N., R. Auckenthaler, M. C. Descombes, M. Bes, F. Vandenesch, and J. Etienne. 2004. Community-acquired methicillin-resistant Staphylococcus aureus isolated in Switzerland contains the Panton-Valentine leukocidin or exfoliative toxin genes. J. Clin. Microbiol. 42:825-828. [PMC free article] [PubMed]
18. Lina, G., Y. Piemont, F. Godail-Gamot, M. Bes, M. O. Peter, V. Gauduchon, F. Vandenesch, and J. Etienne. 1999. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis. 29:1128-1132. [PubMed]
19. Murakami, K., W. Minamide, K. Wada, E. Nakamura, H. Teraoka, and S. Watanabe. 1991. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J. Clin. Microbiol. 29:2240-2244. [PMC free article] [PubMed]
20. Naimi, T. S., K. H. LeDell, K. Como-Sabetti, S. M. Borchardt, D. J. Boxrud, J. Etienne, S. K. Johnson, F. Vandenesch, S. Fridkin, C. O'Boyle, R. N. Danila, and R. Lynfield. 2003. Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA 290:2976-2984. [PubMed]
21. Narita, S., J. Kaneko, J. Chiba, Y. Piemont, S. Jarraud, J. Etienne, and Y. Kamio. 2001. Phage conversion of Panton-Valentine leukocidin in Staphylococcus aureus: molecular analysis of a PVL-converting phage, phiSLT. Gene 268:195-206. [PubMed]
21a. National Committee for Clinical Laboratory Standards. 2000. Methods for dilution antimicrobial susceptibility testing for bacteria that grow aerobically. Approved standard M7-A5. National Committee for Clinical Laboratory Standards, Wayne, Pa.
22. O'Brien, F. G., T. T. Lim, F. N. Chong, G. W. Coombs, M. C. Enright, D. A. Robinson, A. Monk, B. Said-Salim, B. N. Kreiswirth, and W. B. Grubb. 2004. Diversity among community isolates of methicillin-resistant Staphylococcus aureus in Australia. J. Clin. Microbiol. 42:3185-3190. [PMC free article] [PubMed]
23. O'Brien, F. G., J. W. Pearman, M. Gracey, T. V. Riley, and W. B. Grubb. 1999. Community strain of methicillin-resistant Staphylococcus aureus involved in a hospital outbreak. J. Clin. Microbiol. 37:2858-2862. [PMC free article] [PubMed]
24. Okuma, K., K. Iwakawa, J. D. Turnidge, W. B. Grubb, J. M. Bell, F. G. O'Brien, G. W. Coombs, J. W. Pearman, F. C. Tenover, M. Kapi, C. Tiensasitorn, T. Ito, and K. Hiramatsu. 2002. Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J. Clin. Microbiol. 40:4289-4294. [PMC free article] [PubMed]
25. Ramdani-Bouguessa, N., N. Bensafar, and R. Denine. 2001. Susceptibilities of Staphylococcus aureus, Staphylococcus coagulase negative and Enterococcus sp. isolated from an Algerian hospital, abstr. P547. 11th European Congress of Clinical Microbiology and Infectious Diseases.
26. Said-Salim, B., B. Mathema, K. Braughton, S. Davis, D. Sinsimer, W. Eisner, Y. Likhoshvay, F. R. Deleo, and B. N. Kreiswirth. 2005. Differential distribution and expression of Panton-Valentine leukocidin among community-acquired methicillin-resistant Staphylococcus aureus strains. J. Clin. Microbiol. 43:3373-3379. [PMC free article] [PubMed]
27. Saiman, L., M. O'Keefe, P. L. Graham III, F. Wu, B. Said-Salim, B. Kreiswirth, A. LaSala, P. M. Schlievert, and P. Della-Latta. 2003. Hospital transmission of community-acquired methicillin-resistant Staphylococcus aureus among postpartum women. Clin. Infect. Dis. 37:1313-1319. [PubMed]
28. Vandenesch, F., T. Naimi, M. C. Enright, G. Lina, G. R. Nimmo, H. Heffernan, N. Liassine, M. Bes, T. Greenland, M. E. Reverdy, and J. Etienne. 2003. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg. Infect. Dis. 9:978-984. [PMC free article] [PubMed]

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