291
Views
20
CrossRef citations to date
0
Altmetric
Perspective

Staphylococcal vaccine development: review of past failures and plea for a future evaluation of vaccine efficacy not only on staphylococcal infections but also on mucosal carriage

, , , , , & show all
Pages 1249-1259 | Published online: 09 Jan 2014

References

  • Lowy FD. Staphylococcus aureus infections. N. Engl. J. Med. 339(8), 520–532 (1998).
  • David MZ, Daum RS. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin. Microbiol. Rev. 23(3), 616–687 (2010).
  • Daum RS, Spellberg B. Progress toward a Staphylococcus aureus vaccine. Clin. Infect. Dis. 54(4), 560–567 (2012).
  • Noskin GA, Rubin RJ, Schentag JJ et al. National trends in Staphylococcus aureus infection rates: impact on economic burden and mortality over a 6-year period (1998–2003). Clin. Infect. Dis. 45(9), 1132–1140 (2007).
  • Wertheim HF, Vos MC, Ott A et al. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 364(9435), 703–705 (2004).
  • Kluytmans J, van BA, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10(3), 505–520 (1997).
  • Perl TM, Cullen JJ, Wenzel RP et al. Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N. Engl. J. Med. 346(24), 1871–1877 (2002).
  • Berthelot P, Grattard F, Cazorla C et al. Is nasal carriage of Staphylococcus aureus the main acquisition pathway for surgical-site infection in orthopaedic surgery? Eur. J. Clin. Microbiol. Infect. Dis. 29(4), 373–382 (2010).
  • Kluytmans JA, Mouton JW, Ijzerman EP et al. Nasal carriage of Staphylococcus aureus as a major risk factor for wound infections after cardiac surgery. J. Infect. Dis. 171(1), 216–219 (1995).
  • Pujol M, Pena C, Pallares R et al. Nosocomial Staphylococcus aureus bacteremia among nasal carriers of methicillin-resistant and methicillin-susceptible strains. Am. J. Med. 100(5), 509–516 (1996).
  • Corbella X, Dominguez MA, Pujol M et al. Staphylococcus aureus nasal carriage as a marker for subsequent staphylococcal infections in intensive care unit patients. Eur. J. Clin. Microbiol. Infect. Dis. 16(5), 351–357 (1997).
  • Aktas E, Pazarli O, Kulah C, Comert F, Kulah E, Sumbuloglu V. Determination of Staphylococcus aureus carriage in hemodialysis and peritoneal dialysis patients and evaluation of the clonal relationship between carriage and clinical isolates. Am. J. Infect. Control 39(5), 421–425 (2011).
  • Nouwen J, Schouten J, Schneebergen P et al. Staphylococcus aureus carriage patterns and the risk of infections associated with continuous peritoneal dialysis. J. Clin. Microbiol. 44(6), 2233–2236 (2006).
  • Nielsen J, Ladefoged SD, Kolmos HJ. Dialysis catheter-related septicaemia--focus on Staphylococcus aureus septicaemia. Nephrol. Dial. Transplant. 13(11), 2847–2852 (1998).
  • Nguyen MH, Kauffman CA, Goodman RP et al. Nasal carriage of and infection with Staphylococcus aureus in HIV-infected patients. Ann. Intern. Med. 130(3), 221–225 (1999).
  • Squier C, Rihs JD, Risa KJ et al. Staphylococcus aureus rectal carriage and its association with infections in patients in a surgical intensive care unit and a liver transplant unit. Infect. Control Hosp. Epidemiol. 23(9), 495–501 (2002).
  • Safdar N, Bradley EA. The risk of infection after nasal colonization with Staphylococcus aureus. Am. J. Med. 121(4), 310–315 (2008).
  • Simor AE. Staphylococcal decolonisation: an effective strategy for prevention of infection? Lancet Infect. Dis. 11(12), 952–962 (2011).
  • Tacconelli E, Carmeli Y, Aizer A, Ferreira G, Foreman MG, D'Agata EM. Mupirocin prophylaxis to prevent Staphylococcus aureus infection in patients undergoing dialysis: a meta-analysis. Clin. Infect. Dis. 37(12), 1629–1638 (2003).
  • Bode LG, Kluytmans JA, Wertheim HF et al. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N. Engl. J. Med. 362(1), 9–17 (2010).
  • Walsh EE, Greene L, Kirshner R. Sustained reduction in methicillin-resistant Staphylococcus aureus wound infections after cardiothoracic surgery. Arch. Intern. Med. 171(1), 68–73 (2011).
  • Wertheim HF, Vos MC, Ott A et al. Mupirocin prophylaxis against nosocomial Staphylococcus aureus infections in nonsurgical patients: a randomized study. Ann. Intern. Med. 140(6), 419–425 (2004).
  • Kalmeijer MD, Coertjens H, van Nieuwland-Bollen PM et al. Surgical site infections in orthopedic surgery: the effect of mupirocin nasal ointment in a double-blind, randomized, placebo-controlled study. Clin. Infect. Dis. 35(4), 353–358 (2002).
  • Courville XF, Tomek IM, Kirkland KB, Birhle M, Kantor SR, Finlayson SR. Cost-effectiveness of preoperative nasal mupirocin treatment in preventing surgical site infection in patients undergoing total hip and knee arthroplasty: a cost-effectiveness analysis. Infect. Control Hosp. Epidemiol. 33(2), 152–159 (2012).
  • Patel JB, Gorwitz RJ, Jernigan JA. Mupirocin resistance. Clin. Infect. Dis. 49(6), 935–941 (2009).
  • Wang JT, Sheng WH, Wang JL et al. Longitudinal analysis of chlorhexidine susceptibilities of nosocomial methicillin-resistant Staphylococcus aureus isolates at a teaching hospital in Taiwan. J. Antimicrob. Chemother. 62(3), 514–517 (2008).
  • Fattom AI, Sarwar J, Ortiz A, Naso R. A Staphylococcus aureus capsular polysaccharide (CP) vaccine and CP-specific antibodies protect mice against bacterial challenge. Infect. Immun. 64(5), 1659–1665 (1996).
  • Shinefield H, Black S, Fattom A et al. Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. N. Engl. J. Med. 346(7), 491–496 (2002).
  • Creech CB, Johnson BG, Alsentzer AR, Hohenboken M, Edwards KM, Talbot TRIII. Vaccination as infection control: a pilot study to determine the impact of Staphylococcus aureus vaccination on nasal carriage. Vaccine 28(1), 256–260 (2009).
  • Pishchany G, McCoy AL, Torres VJ et al. Specificity for human hemoglobin enhances Staphylococcus aureus infection. Cell Host. Microbe. 8(6), 544–550 (2010).
  • Kuklin NA, Clark DJ, Secore S et al. 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(4), 2215–2223 (2006).
  • Etz H, Minh DB, Henics T et al. Identification of in vivo expressed vaccine candidate antigens from Staphylococcus aureus. Proc. Natl Acad. Sci. USA 99(10), 6573–6578 (2002).
  • Zorman JK, Esser M, Raedler M et al. Naturally occurring IgG antibody levels to the Staphylococcus aureus protein IsdB in humans. Hum. Vaccin. Immunother. 9(9), doi:10.4161/hv.25253 (2013) (Epub ahead of print).
  • Patti JM. Will we ever see the approval of a Staphylococcus aureus vaccine? Expert Rev. Anti. Infect. Ther. 9(10), 845–846 (2011).
  • Fowler VG, Allen KB, Moreira ED et al. Effect of an investigational vaccine for preventing Staphylococcus aureus infections after cardiothoracic surgery: a randomized trial. JAMA 309(13), 1368–1378 (2013).
  • Maira-Litran T, Kropec A, Abeygunawardana C et al. Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect. Immun. 70(8), 4433–4440 (2002).
  • Skurnik D, Kropec A, Roux D, Theilacker C, Huebner J, Pier GB. Natural antibodies in normal human serum inhibit staphylococcus aureus capsular polysaccharide vaccine efficacy. Clin. Infect. Dis. 55(9), 1188–1197 (2012).
  • Skurnik D, Merighi M, Grout M et al. Animal and human antibodies to distinct Staphylococcus aureus antigens mutually neutralize opsonic killing and protection in mice. J. Clin. Invest 120(9), 3220–3233 (2010).
  • Nanra JS, Buitrago SM, Crawford S et al. Capsular polysaccharides are an important immune evasion mechanism for Staphylococcus aureus. Hum. Vaccin. Immunother. 9(3), doi:10.4161/hv.23223 (2012) (Epub ahead of print).
  • Grigg JC, Ukpabi G, Gaudin CF, Murphy ME. Structural biology of heme binding in the Staphylococcus aureus Isd system. J. Inorg. Biochem. 104(3), 341–348 (2010).
  • Hurd AF, Garcia-Lara J, Rauter Y, Cartron M, Mohamed R, Foster SJ. The iron-regulated surface proteins IsdA, IsdB, and IsdH are not required for heme iron utilization in Staphylococcus aureus. FEMS Microbiol. Lett. 329(1), 93–100 (2012).
  • Hawkins J, Kodali S, Matsuka YV et al. A recombinant clumping factor A-containing vaccine induces functional antibodies to Staphylococcus aureus that are not observed after natural exposure. Clin. Vaccine Immunol. 19(10), 1641–1650 (2012).
  • Novick RP. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48(6), 1429–1449 (2003).
  • Wertheim HF, Walsh E, Choudhurry R et al. Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med. 5(1), e17 (2008).
  • Tong A, Tong SY, Zhang Y et al. Panton-Valentine leukocidin is not the primary determinant of outcome for Staphylococcus aureus skin infections: evaluation from the CANVAS studies. PLoS ONE 7(5), e37212 (2012).
  • Kahl BC, Belling G, Becker P et al. Thymidine-dependent Staphylococcus aureus small-colony variants are associated with extensive alterations in regulator and virulence gene expression profiles. Infect. Immun. 73(7), 4119–4126 (2005).
  • Gagnaire J, Dauwalder O, Boisset S et al. Detection of Staphylococcus aureus delta-toxin production by whole-cell MALDI-TOF mass spectrometry. PLoS ONE 7(7), e40660 (2012).
  • Luedicke C, Slickers P, Ehricht R, Monecke S. Molecular fingerprinting of Staphylococcus aureus from bone and joint infections. Eur. J. Clin. Microbiol. Infect. Dis. 29(4), 457–463 (2010).
  • Lina G, Piemont Y, Godail-Gamot F et al. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis. 29(5), 1128–1132 (1999).
  • Spellberg B, Ibrahim AS, Yeaman MR et al. The antifungal vaccine derived from the recombinant N terminus of Als3p protects mice against the bacterium Staphylococcus aureus. Infect. Immun. 76(10), 4574–4580 (2008).
  • Verkaik NJ, Benard M, Boelens HA et al. Immune evasion cluster-positive bacteriophages are highly prevalent among human Staphylococcus aureus strains, but they are not essential in the first stages of nasal colonization. Clin. Microbiol. Infect. 17(3), 343–348 (2011).
  • Rooijakkers SH, Ruyken M, Roos A et al. Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat. Immunol. 6(9), 920–927 (2005).
  • Rooijakkers SH, van Kessel KP, van Strijp JA. Staphylococcal innate immune evasion. Trends Microbiol. 13(12), 596–601 (2005).
  • van Wamel WJ, Rooijakkers SH, Ruyken M, van Kessel KP, van Strijp JA. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J. Bacteriol. 188(4), 1310–1315 (2006).
  • Postma B, Poppelier MJ, van Galen JC et al. Chemotaxis inhibitory protein of Staphylococcus aureus binds specifically to the C5a and formylated peptide receptor. J. Immunol. 172(11), 6994–7001 (2004).
  • Rahimpour R, Mitchell G, Khandaker MH et al. Bacterial superantigens induce down-modulation of CC chemokine responsiveness in human monocytes via an alternative chemokine ligand-independent mechanism. J. Immunol. 162(4), 2299–2307 (1999).
  • Jin T, Bokarewa M, Foster T, Mitchell J, Higgins J, Tarkowski A. Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J. Immunol. 172(2), 1169–1176 (2004).
  • Abel J, Goldmann O, Ziegler C et al. Staphylococcus aureus evades the extracellular antimicrobial activity of mast cells by promoting its own uptake. J. Innate. Immun. 3(5), 495–507 (2011).
  • Brown EL, Dumitrescu O, Thomas D et al. The Panton-Valentine leukocidin vaccine protects mice against lung and skin infections caused by Staphylococcus aureus USA300. Clin. Microbiol. Infect. 15(2), 156–164 (2009).
  • Quinn GA, Cole AM. Suppression of innate immunity by a nasal carriage strain of Staphylococcus aureus increases its colonization on nasal epithelium. Immunology 122(1), 80–89 (2007).
  • Cole AM, Tahk S, Oren A et al. Determinants of Staphylococcus aureus nasal carriage. Clin. Diagn. Lab Immunol. 8(6), 1064–1069 (2001).
  • Quinn GA, Tarwater PM, Cole AM. Subversion of interleukin-1-mediated host defence by a nasal carrier strain of Staphylococcus aureus. Immunology 128(1 Suppl.), e222–e229 (2009).
  • Muthukrishnan G, Quinn GA, Lamers RP et al. Exoproteome of Staphylococcus aureus reveals putative determinants of nasal carriage. J. Proteome. Res. 10(4), 2064–2078 (2011).
  • Burnside K, Lembo A, Harrell MI et al. Vaccination With a UV-irradiated genetically attenuated Mutant of Staphylococcus aureus Provides protection against subsequent systemic infection. J. Infect. Dis. 206(11), 1734–1744 (2012).
  • Andrews WW, Schelonka R, Waites K, Stamm A, Cliver SP, Moser S. Genital tract methicillin-resistant Staphylococcus aureus: risk of vertical transmission in pregnant women. Obstet. Gynecol. 111(1), 113–118 (2008).
  • Quinti I, Soresina A, Spadaro G et al. Long-term follow-up and outcome of a large cohort of patients with common variable immunodeficiency. J. Clin. Immunol. 27(3), 308–316 (2007).
  • Oksenhendler E, Gerard L, Fieschi C et al. Infections in 252 patients with common variable immunodeficiency. Clin. Infect. Dis. 46(10), 1547–1554 (2008).
  • Song E, Jaishankar GB, Saleh H, Jithpratuck W, Sahni R, Krishnaswamy G. Chronic granulomatous disease: a review of the infectious and inflammatory complications. Clin. Mol. Allergy 9(1), 10 (2011).
  • Hartl D, Lehmann N, Hoffmann F et al. Dysregulation of innate immune receptors on neutrophils in chronic granulomatous disease. J. Allergy Clin. Immunol. 121(2), 375–382 (2008).
  • Milner JD, Brenchley JM, Laurence A et al. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 452(7188), 773–776 (2008).
  • Ma CS, Chew GY, Simpson N et al. Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J. Exp. Med. 205(7), 1551–1557 (2008).
  • Ishigame H, Kakuta S, Nagai T et al. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30(1), 108–119 (2009).
  • Puel A, Cypowyj S, Bustamante J et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332(6025), 65–68 (2011).
  • Nembrini C, Marsland BJ, Kopf M. IL-17-producing T cells in lung immunity and inflammation. J. Allergy Clin. Immunol. 123(5), 986–994 (2009).
  • Cho JS, Pietras EM, Garcia NC et al. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J. Clin. Invest 120(5), 1762–1773 (2010).
  • Lin L, Ibrahim AS, Xu X et al. Th1-Th17 cells mediate protective adaptive immunity against Staphylococcus aureus and Candida albicans infection in mice. PLoS Pathog. 5(12), e1000703 (2009).
  • Archer NK, Harro JM, Shirtliff ME. Clearance of Staphylococcus aureus nasal carriage is T-cell dependent and mediated through IL-17A expression and neutrophil influx. Infect. Immun. 81(6), 2070–2075 (2013).
  • Projan SJ, Nesin M, Dunman PM. Staphylococcal vaccines and immunotherapy: to dream the impossible dream? Curr. Opin. Pharmacol. 6(5), 473–479 (2006).
  • Kim HK, Kim HY, Schneewind O, Missiakas D. Identifying protective antigens of Staphylococcus aureus, a pathogen that suppresses host immune responses. FASEB J. 25(10), 3605–3612 (2011).
  • Sabat A, Melles DC, Martirosian G, Grundmann H, van BA, Hryniewicz W. Distribution of the serine-aspartate repeat protein-encoding sdr genes among nasal-carriage and invasive Staphylococcus aureus strains. J. Clin. Microbiol. 44(3), 1135–1138 (2006).
  • Adhikari RP, Karauzum H, Sarwar J et al. Novel structurally designed vaccine for S. aureus alpha-hemolysin: Protection against bacteremia and pneumonia. PLoS ONE 7(6), e38567 (2012).
  • Seib KL, Zhao X, Rappuoli R. Developing vaccines in the era of genomics: a decade of reverse vaccinology. Clin. Microbiol. Infect. 18( Suppl. 5), 109–116 (2012).
  • Oprea M, Antohe F. Reverse-vaccinology strategy for designing T-cell epitope candidates for Staphylococcus aureus endocarditis vaccine. Biologicals 41(3), 148–153 (2013).
  • Patti JM. A humanized monoclonal antibody targeting Staphylococcus aureus. Vaccine 22( Suppl. 1), S39–S43 (2004).
  • Liu C, Graber CJ, Karr M et al. A population-based study of the incidence and molecular epidemiology of methicillin-resistant Staphylococcus aureus disease in San Francisco, 2004–2005. Clin. Infect. Dis. 46(11), 1637–1646 (2008).
  • Duffy J, Dumyati G, Bulens S et al. Community-onset invasive methicillin-resistant Staphylococcus aureus infections following hospital discharge. Am. J. Infect. Control 41(9), 782–786 (2013).
  • Pier GB. Will there ever be a universal Staphylococcus aureus vaccine? Hum. Vaccin. Immunother. 9(9) (2013).
  • Acton DS, Plat-Sinnige MJ, van WW, de GN, van BA. 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(2), 115–127 (2009).
  • Mertz D, Frei R, Jaussi B et al. Throat swabs are necessary to reliably detect carriers of Staphylococcus aureus. Clin. Infect. Dis. 45(4), 475–477 (2007).
  • Verhoeven PO, Grattard F, Carricajo A et al. An algorithm based on one or two nasal samples is accurate to identify persistent nasal carriers of Staphylococcus aureus. Clin. Microbiol. Infect. 18(6), 551–557 (2012).
  • Nouwen JL, Fieren MW, Snijders S, Verbrugh HA, van BA. Persistent (not intermittent) nasal carriage of Staphylococcus aureus is the determinant of CPD-related infections. Kidney Int. 67(3), 1084–1092 (2005).
  • van Belkum A, Verkaik NJ, de Vogel CP et al. Reclassification of Staphylococcus aureus nasal carriage types. J. Infect. Dis. 199(12), 1820–1826 (2009).
  • Kalmeijer MD, van Nieuwland-Bollen E, Bogaers-Hofman D, de Baere GA. Nasal carriage of Staphylococcus aureus is a major risk factor for surgical-site infections in orthopedic surgery. Infect. Control Hosp. Epidemiol. 21(5), 319–323 (2000).
  • Verhoeven PO, Grattard F, Carricajo A et al. Quantification by real-time PCR assay of Staphylococcus aureus load: a useful tool for rapidly identifying persistent nasal carriers. J. Clin. Microbiol. 50(6), 2063–2065 (2012).
  • Roca A, Bottomley C, Hill PC et al. Effect of age and vaccination with a pneumococcal conjugate vaccine on the density of pneumococcal nasopharyngeal carriage. Clin. Infect. Dis. 55(6), 816–824 (2012).
  • Lu YJ, Gross J, Bogaert D et al. Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog. 4(9), e1000159 (2008).
  • Lemon KP, Klepac-Ceraj V, Schiffer HK, Brodie EL, Lynch SV, Kolter R. Comparative analyses of the bacterial microbiota of the human nostril and oropharynx. mBio. 1(3), e00129–10 (2010).
  • Frank DN, Feazel LM, Bessesen MT, Price CS, Janoff EN, Pace NR. The human nasal microbiota and Staphylococcus aureus carriage. PLoS ONE 5(5), e10598 (2010).
  • Iwase T, Uehara Y, Shinji H et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465(7296), 346–349 (2010).
  • Dunne EM, Smith-Vaughan HC, Robins-Browne RM, Mulholland EK, Satzke C. Nasopharyngeal microbial interactions in the era of pneumococcal conjugate vaccination. Vaccine 31(19), 2333–2342 (2013).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.