Rhesus macaques (macaca mulatta) are natural hosts of specific staphylococcus aureus lineages

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  van den Berg, Sanne ^a   van Wamel, Willem J B ^a   Snijders, Susan V ^a   Ouwerling, Boudewijn ^b   de Vogel, Corné P ^a   Boelens, Hélène A ^a   Willems, Rob J L ^c   Huijsdens, Xander W ^d   Verreck, Frank A W ^b   Kondova, Ivanela ^b   Heidt, Peter J ^b   Verbrugh, Henri A ^a   van Belkum, Alex ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G;

AGR GENE; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL TRANSMISSION; BACTERIUM ISOLATION; BLOOD ANALYSIS; CONTROLLED STUDY; DISEASE CARRIER; GENE IDENTIFICATION; GENE SEQUENCE; GENOTYPE; HOST PATHOGEN INTERACTION; HUMAN VERSUS ANIMAL COMPARISON; MULTILOCUS SEQUENCE TYPING; NATURAL HOST; NONHUMAN; NOSE SMEAR; POLYMERASE CHAIN REACTION; PULSED FIELD GEL ELECTROPHORESIS; RHESUS MONKEY; SPA GENE; STAPHYLOCOCCUS AUREUS; ANIMAL; BLOOD; GENETICS; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; MACACA MULATTA; MICROBIOLOGY; MOLECULAR EVOLUTION; NOSE; PHYLOGENY; SPECIES DIFFERENCE;

ANIMALIA; MACACA; MACACA MULATTA; STAPHYLOCOCCUS AUREUS;

ANIMALS; EVOLUTION, MOLECULAR; GENES, BACTERIAL; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; MACACA MULATTA; NOSE; PHYLOGENY; SPECIES SPECIFICITY; STAPHYLOCOCCUS AUREUS;

EID: 80054775966     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026170     Document Type: Article

References (48)

1. Needham AJ, Kibart M, Crossley H, Ingham PW, Foster SJ, (2004) Drosophila melanogaster as a model host for Staphylococcus aureus infection. Microbiology 150: 2347-2355.
2. Sifri CD, Begun J, Ausubel FM, Calderwood SB, (2003) Caenorhabditis elegans as a model host for Staphylococcus aureus pathogenesis. Infect Immun 71: 2208-2217.
3. Tarkowski A, Collins LV, Gjertsson I, Hultgren OH, Jonsson IM, et al. (2001) Model systems: modeling human staphylococcal arthritis and sepsis in the mouse. Trends Microbiol 9: 321-326.
4. Collins LV, Tarkowski A, (2006) Animal models of experimental Staphylococcus aureus infection. In: Fischetti VA, Novick RP, Ferreti JJ, Portnoy DA, Rood JI, editors. Gram-positive pathogens Washington ASM Press pp. 535-543.
5. van Belkum A, Melles DC, Peeters JK, van Leeuwen WB, van Duijkeren E, et al. (2008) Methicillin-resistant and-susceptible Staphylococcus aureus sequence type 398 in pigs and humans. Emerg Infect Dis 14: 479-483.
6. Wulf M, Voss A, (2008) MRSA in livestock animals-an epidemic waiting to happen? Clin Microbiol Infect 14: 519-521.
7. Fitzgerald JR, Monday SR, Foster TJ, Bohach GA, Hartigan PJ, et al. (2001) Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol 183: 63-70.
8. Herron LL, Chakravarty R, Dwan C, Fitzgerald JR, Musser JM, et al. (2002) Genome sequence survey identifies unique sequences and key virulence genes with unusual rates of amino acid substitution in bovine Staphylococcus aureus. Infect Immun 70: 3978-3981.
9. van Cleef BA, Graveland H, Haenen AP, van de Giessen AW, Heederik D, et al. (2011) Persistence of livestock-associated methicillin-resistant Staphylococcus aureus in field workers after short-term occupational exposure to pigs and veal calves. J Clin Microbiol 49: 1030-1033.
10. Kuklin NA, Clark DJ, Secore S, Cook J, Cope LD, et al. (2006) A novel Staphylococcus aureus vaccine: iron surface determinant B induces rapid antibody responses in rhesus macaques and specific increased survival in a murine S. aureus sepsis model. Infect Immun 74: 2215-2223.
11. LeClaire RD, Hunt RE, Bavari S, (2002) Protection against bacterial superantigen staphylococcal enterotoxin B by passive vaccination. Infect Immun 70: 2278-2281.
12. Lu Q, Li Y, Wen L, Guo S, Chen Y, et al. (2003) Safety evaluation of recombinant staphylokinase in rhesus monkeys. Toxicol Pathol 31: 14-21.
13. Verkaik NJ, Boelens HA, de Vogel CP, Tavakol M, Bode LG, et al. (2010) Heterogeneity of the humoral immune response following Staphylococcus aureus bacteremia. Eur J Clin Microbiol Infect Dis 29: 509-518.
14. Verkaik NJ, de Vogel CP, Boelens HA, Grumann D, Hoogenboezem T, et al. (2009) Anti-staphylococcal humoral immune response in persistent nasal carriers and noncarriers of Staphylococcus aureus. J Infect Dis 199: 625-632.
15. Koning S, van Belkum A, Snijders S, van Leeuwen W, Verbrugh H, et al. (2003) Severity of nonbullous Staphylococcus aureus impetigo in children is associated with strains harboring genetic markers for exfoliative toxin B, Panton-Valentine leukocidin, and the multidrug resistance plasmid pSK41. J Clin Microbiol 41: 3017-3021.
16. Martins TB, Augustine NH, Hill HR, (2006) Development of a multiplexed fluorescent immunoassay for the quantitation of antibody responses to group A streptococci. J Immunol Methods 316: 97-106.
17. Verkaik N, Brouwer E, Hooijkaas H, van Belkum A, van Wamel W, (2008) Comparison of carboxylated and Penta-His microspheres for semi-quantitative measurement of antibody responses to His-tagged proteins. J Immunol Methods 335: 121-125.
18. Melles DC, Gorkink RF, Boelens HA, Snijders SV, Peeters JK, et al. (2004) Natural population dynamics and expansion of pathogenic clones of Staphylococcus aureus. J Clin Invest 114: 1732-1740.
19. Aires-de-Sousa M, Boye K, de Lencastre H, Deplano A, Enright MC, et al. (2006) High interlaboratory reproducibility of DNA sequence-based typing of bacteria in a multicenter study. J Clin Microbiol 44: 619-621.
20. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG, (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38: 1008-1015.
21. Francisco AP, Bugalho M, Ramirez M, Carrico JA, (2009) Global optimal eBURST analysis of multilocus typing data using a graphic matroid approach. BMC Bioinformatics 10: 152.
22. Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, et al. (1991) Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol 29: 2240-2244.
23. Holtfreter S, Grumann D, Schmudde M, Nguyen HT, Eichler P, et al. (2007) Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J Clin Microbiol 45: 2669-2680.
24. Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, et al. (2002) Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 70: 631-641.
25. Tristan A, Ying L, Bes M, Etienne J, Vandenesch F, et al. (2003) Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. J Clin Microbiol 41: 4465-4467.
26. van Wamel WJ, Rooijakkers SH, Ruyken M, van Kessel KP, van Strijp JA, (2006) The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J Bacteriol 188: 1310-1315.
27. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, et al. (2004) Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 10: 243-245.
28. Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, et al. (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5: 751-762.
29. Kalmeijer MD, Coertjens H, van Nieuwland-Bollen PM, Bogaers-Hofman D, de Baere GA, et al. (2002) Surgical site infections in orthopedic surgery: the effect of mupirocin nasal ointment in a double-blind, randomized, placebo-controlled study. Clin Infect Dis 35: 353-358.
30. Perl TM, Cullen JJ, Wenzel RP, Zimmerman MB, Pfaller MA, et al. (2002) Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N Engl J Med 346: 1871-1877.
31. von Eiff C, Becker K, Machka K, Stammer H, Peters G, (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med 344: 11-16.
32. Bode LG, Kluytmans JA, Wertheim HF, Bogaers D, Vandenbroucke-Grauls CM, et al. (2010) Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N Engl J Med 362: 9-17.
33. Kluytmans J, van Belkum A, Verbrugh H, (1997) Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10: 505-520.
34. Williams RE, (1963) Healthy carriage of Staphylococcus aureus: its prevalence and importance. Bacteriol Rev 27: 56-71.
35. Wertheim HF, Verveer J, Boelens HA, van Belkum A, Verbrugh HA, et al. (2005) Effect of mupirocin treatment on nasal, pharyngeal, and perineal carriage of Staphylococcus aureus in healthy adults. Antimicrob Agents Chemother 49: 1465-1467.
36. Acton DS, Plat-Sinnige MJ, van Wamel W, de Groot N, van Belkum A, (2009) Intestinal carriage of Staphylococcus aureus: how does its frequency compare with that of nasal carriage and what is its clinical impact? Eur J Clin Microbiol Infect Dis 28: 115-127.
37. Mertz D, Frei R, Jaussi B, Tietz A, Stebler C, et al. (2007) Throat swabs are necessary to reliably detect carriers of Staphylococcus aureus. Clin Infect Dis 45: 475-477.
38. Leigh DA, Joy G, (1993) Treatment of familial staphylococcal infection-comparison of mupirocin nasal ointment and chlorhexidine/neomycin (Naseptin) cream in eradication of nasal carriage. J Antimicrob Chemother 31: 909-917.
39. Watanakunakorn C, Axelson C, Bota B, Stahl C, (1995) Mupirocin ointment with and without chlorhexidine baths in the eradication of Staphylococcus aureus nasal carriage in nursing home residents. Am J Infect Control 23: 306-309.
40. Wertheim HF, Walsh E, Choudhurry R, Melles DC, Boelens HA, et al. (2008) Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med 5: e17.
41. Eriksen NH, Espersen F, Rosdahl VT, Jensen K, (1995) Carriage of Staphylococcus aureus among 104 healthy persons during a 19-month period. Epidemiol Infect 115: 51-60.
42. Hu L, Umeda A, Kondo S, Amako K, (1995) Typing of Staphylococcus aureus colonising human nasal carriers by pulsed-field gel electrophoresis. J Med Microbiol 42: 127-132.
43. Thomas D, Chou S, Dauwalder O, Lina G, (2007) Diversity in Staphylococcus aureus enterotoxins. Chem Immunol Allergy 93: 24-41.
44. Becker K, Friedrich AW, Lubritz G, Weilert M, Peters G, et al. (2003) Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J Clin Microbiol 41: 1434-1439.
45. Collery MM, Smyth DS, Twohig JM, Shore AC, Coleman DC, et al. (2008) Molecular typing of nasal carriage isolates of Staphylococcus aureus from an Irish university student population based on toxin gene PCR, agr locus types and multiple locus, variable number tandem repeat analysis. J Med Microbiol 57: 348-358.
46. Noble WC, Williams RE, Jevons MP, Shooter RA, (1964) Some aspects of nasal carriage of staphylococci. J Clin Pathol 17: 79-83.
47. Clarke SR, Brummell KJ, Horsburgh MJ, McDowell PW, Mohamad SA, et al. (2006) Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J Infect Dis 193: 1098-1108.
48. Dryla A, Prustomersky S, Gelbmann D, Hanner M, Bettinger E, et al. (2005) Comparison of antibody repertoires against Staphylococcus aureus in healthy individuals and in acutely infected patients. Clin Diagn Lab Immunol 12: 387-398.