Skip to main content
Log in

Overview of the risks of Staphylococcus aureus infections and their control by bacteriophages and bacteriophage-encoded products

  • Clinical Microbiology - Review
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Staphylococcus aureus is the leading cause of secondary infections in hospitals and a challenging pathogen in food industries. Decades after it was first reported, β-lactam-resistant S. aureus remains a subject of intense research owing to the ever-increasing issue of drug resistance. S. aureus bacteriophages (phages) or their encoded products are considered an alternative to antibiotics as they have been shown to be effective in treating some S. aureus-associated infections. In this review, we present a concise collection of the literature on the pathogenic potential of S. aureus and examine the prospects of using S. aureus phages and their encoded products as antimicrobials.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339(8):520–532. https://doi.org/10.1056/NEJM199808203390806

    Article  CAS  PubMed  Google Scholar 

  2. Williams REO (1963) Healthy carriage of Staphylococcus aureus: its prevalence and importance. Bacteriol Rev 27(1):56

    Article  CAS  Google Scholar 

  3. Wertheim HF, Melles DC, Vos MC, Van Leeuwen W, Van Belkum A, Verbrugh HA, Nouwen JL (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5(12):751–762. https://doi.org/10.1016/S1473-3099(05)70295-4

    Article  PubMed  Google Scholar 

  4. Taylor TA, Unakal CG (2020) Staphylococcus aureus. [Updated 2020 Aug 23]. In: StatPearls. StatPearls Publishing, Treasure Island (FL). Available from: https://www.ncbi.nlm.nih.gov/books/NBK441868/

  5. Foster T (1996) Staphylococcus. In: Baron S (ed) Medical Microbiology, 4th edn. The University of Texas Medical Branch, Galveston, pp 187–197

    Google Scholar 

  6. Wilde AD, Snyder DJ, Putnam NE, Valentino MD, Hammer ND, Lonergan ZR et al (2015) Bacterial hypoxic responses revealed as critical determinants of the host-pathogen outcome by TnSeq analysis of Staphylococcus aureus invasive infection. PLoS Pathog 11(12):e1005341. https://doi.org/10.1371/journal.ppat.1005341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. McGuinness WA, Malachowa N, DeLeo FR (2017) Focus: infectious diseases: vancomycin-resistance in Staphylococcus aureus. Yale J Biol Med 90(2):269–281

    CAS  PubMed  PubMed Central  Google Scholar 

  8. WHO (2020) Global action plan on AMR https://www.who.int/antimicrobial-resistance/global-action-plan/en/ accessed 29 January 2020

  9. Úbeda C, Maiques E, Knecht E, Lasa Í, Novick RP, Penadés JR (2005) Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol Microbiol 56(3):836–844. https://doi.org/10.1111/j.1365-2958.2005.04584.x

    Article  CAS  PubMed  Google Scholar 

  10. Singh R, Sripada L, Singh R (2014) Side effects of antibiotics during bacterial infection: mitochondria, the main target in host cell. Mitochondrion 16:50–54. https://doi.org/10.1016/j.mito.2013.10.005

    Article  CAS  PubMed  Google Scholar 

  11. Keeney KM, Yurist-Doutsch S, Arrieta MC, Finlay BB (2014) Effects of antibiotics on human microbiota and subsequent disease. Annu Rev Microbiol 68:217–235. https://doi.org/10.1146/annurev-micro-091313-103456

    Article  CAS  PubMed  Google Scholar 

  12. Pantosti A, Sanchini A, Monaco M (2007) Mechanisms of antibiotic resistance in Staphylococcus aureus. Future Microbiol 2:323–334. https://doi.org/10.2217/17460913.2.3.323

    Article  CAS  PubMed  Google Scholar 

  13. CDC (2019) Vital signs www.cdc.gov/vitalsigns/staph/index.html accessed on 05 April 2021

  14. Diekema DJ, Pfaller MA, Shortridge D, Zervos M, Jones RN (2019) Twenty-year trends in antimicrobial susceptibilities among Staphylococcus aureus from the SENTRY Antimicrobial Surveillance Program. Open Forum Infect Dis 6(Suppl 1):S47–S53. https://doi.org/10.1093/ofid/ofy270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance accessed on 05 April 2021

  16. Furfaro LL, Payne MS, Chang BJ (2018) Bacteriophage therapy: clinical trials and regulatory hurdles. Front Cell Infect Microbiol 8:376. https://doi.org/10.3389/fcimb.2018.00376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Merril CR, Scholl D, Adhya SL (2003) The prospect for bacteriophage therapy in Western medicine. Nat Rev Drug Discov 2(6):489–497. https://doi.org/10.1038/nrd1111

    Article  CAS  PubMed  Google Scholar 

  18. Deghorain M, Van Melderen L (2012) The Staphylococci phages family: an overview. Viruses 4(12):3316–3335. https://doi.org/10.3390/v4123316

    Article  PubMed  PubMed Central  Google Scholar 

  19. Lyon BR, Skurray RON (1987) Antimicrobial resistance of Staphylococcus aureus: genetic basis. Microbiol Rev 51(1):88–134

    Article  CAS  Google Scholar 

  20. Morikawa K, Takemura AJ, Inose Y, Tsai M, Ohta T, Msadek T (2012) Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus. PLoS Pathog 8(11):e1003003. https://doi.org/10.1371/journal.ppat.1003003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Everitt RG, Didelot X, Batty EM, Miller RR, Knox K, Young BC, Bowden R, Auton A, Votintseva A, Larner-Svensson H, Charlesworth J (2014) Mobile elements drive recombination hotspots in the core genome of Staphylococcus aureus. Nat Commun 5(1):1–9. https://doi.org/10.1038/ncomms4956

    Article  CAS  Google Scholar 

  22. Alibayov B, Zdenkova K, Sykorova H, Demnerova K (2014) Molecular analysis of Staphylococcus aureus pathogenicity islands (SaPI) and their superantigens combination of food samples. J Microbiol Methods 107:197–204. https://doi.org/10.1016/j.mimet.2014.10.014

    Article  CAS  PubMed  Google Scholar 

  23. Grundstad ML, Parlet CP, Kwiecinski JM, Kavanaugh JS, Crosby HA, Cho YS, Heilmann K, Diekema DJ, Horswill AR (2019) Quorum sensing, virulence, and antibiotic resistance of USA100 methicillin-resistant Staphylococcus aureus isolates. mSphere 4(4):e00553-19. https://doi.org/10.1128/mSphere.00553-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Jarraud S, Lyon GJ, Figueiredo AMS, Lina G, Vandenesch F, Etienne J, Muir TW, Novick RP (2011) Exfoliatin-producing strains define a fourth agr specificity group in Staphylococcus aureus. J Bacteriol 193(24):7027. https://doi.org/10.1128/JB.06355-11

    Article  CAS  PubMed Central  Google Scholar 

  25. Cheung AL, Nishina KA, Trotonda MP, Tamber S (2008) The SarA protein family of Staphylococcus aureus. Int J Biochem Cell Biol 40(3):355–361. https://doi.org/10.1016/j.biocel.2007.10.032

    Article  CAS  PubMed  Google Scholar 

  26. Pichon C, Felden B (2005) Small RNA genes expressed from Staphylococcus aureus genomic and pathogenicity islands with specific expression among pathogenic strains. PNAS 102(40):14249–14254. https://doi.org/10.1073/pnas.0503838102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Desgranges E, Marzi K, Moreau K, Romby P, Caldelari I (2019) Chapter 35 Noncoding RNA. In: Fischetti VA, Novick RP, Ferretti JJ, Portnoy DA, Braunstein M, Rood JI (eds) Gram-positive Pathogens, 3rd edn. Wiley, New York

    Google Scholar 

  28. Haaber J, Penadés JR, Ingmer H (2017) Transfer of antibiotic resistance in Staphylococcus aureus. Trends Microbiol 25(11):893–905. https://doi.org/10.1016/j.tim.2017.05.011

    Article  CAS  PubMed  Google Scholar 

  29. Deurenberg RH, Stobberingh EE (2008) The evolution of Staphylococcus aureus. Infect Genet Evol 8(6):747–763. https://doi.org/10.1016/j.meegid.2008.07.007

    Article  CAS  PubMed  Google Scholar 

  30. Baig S, Johannesen TB, Overballe-Petersen S, Larsen J, Larsen AR, Stegger M (2018) Novel SCCmec type XIII (9A) identified in an ST152 methicillin-resistant Staphylococcus aureus. Infect Genet Evol 61:74–76. https://doi.org/10.1016/j.meegid.2018.03.013

    Article  CAS  PubMed  Google Scholar 

  31. David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23(3):616–687. https://doi.org/10.1128/cmr.00081-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Boucher HW, Corey GR (2008) Epidemiology of methicillin-resistant Staphylococcus aureus. Clin Infect Dis 46(Supplement 5):S344–S349. https://doi.org/10.1086/533590

    Article  PubMed  Google Scholar 

  33. Pantosti A (2012) Methicillin-resistant Staphylococcus aureus associated with animals and its relevance to human health. Front Microbiol 3:127. https://doi.org/10.3389/fmicb.2012.00127

    Article  PubMed  PubMed Central  Google Scholar 

  34. Verstappen KM, Tulinski P, Duim B, Fluit AC, Carney J, Van Nes A, Wagenaar JA (2016) The effectiveness of bacteriophages against methicillin-resistant Staphylococcus aureus ST398 nasal colonization in pigs. PLoS ONE 11(8):e0160242. https://doi.org/10.1371/journal.pone.0160242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Figueiredo AMS, Ferreira FA (2014) The multifaceted resources and microevolution of the successful human and animal pathogen methicillin-resistant Staphylococcus aureus. Mem Inst Oswaldo Cruz 109(3):265–278. https://doi.org/10.1590/0074-0276140016

    Article  PubMed  PubMed Central  Google Scholar 

  36. Montgomery CP, Boyle-Vavra S, Adem PV, Lee JC, Husain AN, Clasen J, Daum RS (2008) Comparison of virulence in community-associated methicillin-resistant Staphylococcus aureus pulsotypes USA300 and USA400 in a rat model of pneumonia. J Infect Dis 198(4):561–570. https://doi.org/10.1086/590157

    Article  CAS  PubMed  Google Scholar 

  37. Xia G, Wolz C (2014) Phages of Staphylococcus aureus and their impact on host evolution. Infect Genet Evol 21:593–601. https://doi.org/10.1016/j.meegid.2013.04.022

    Article  CAS  PubMed  Google Scholar 

  38. Kwan T, Liu J, DuBow M, Gros P, Pelletier J (2005) The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc Natl Acad Sci USA 102(14):5174–5179. https://doi.org/10.1073/pnas.0501140102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Oliveira H, Sampaio M, Melo LD, Dias O, Pope WH, Hatfull GF, Azeredo J (2019) Staphylococci phages display vast genomic diversity and evolutionary relationships. BMC Genomics 20(1):357. https://doi.org/10.1186/s12864-019-5647-8

    Article  PubMed  PubMed Central  Google Scholar 

  40. O’Flaherty S, Coffey A, Edwards R, Meaney W, Fitzgerald GF, Ross RP (2004) Genome of staphylococcal phage K: a new lineage of Myoviridae infecting Gram-positive bacteria with a low G+ C content. J Bacteriol 186(9):2862–2871. https://doi.org/10.1128/JB.186.9.2862-2871.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Goerke C, Pantucek R, Holtfreter S, Schulte B, Zink M, Grumann D, Bröker BM, Doskar J, Wolz C (2009) Diversity of prophages in dominant Staphylococcus aureus clonal lineages. J Bacteriol 191(11):3462–3468. https://doi.org/10.1128/jb.01804-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Chang Y, Shin H, Lee JH, Park CJ, Paik SY, Ryu S (2015) Isolation and genome characterization of the virulent Staphylococcus aureus bacteriophage SA97. Viruses 7(10):5225–5242. https://doi.org/10.3390/v7102870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Głowacka-Rutkowska A, Gozdek A, Empel J, Gawor J, Żuchniewicz K, Kozińska A, Dębski J, Gromadka R, Łobocka M (2019) The ability of lytic staphylococcal podovirus vB_SauP_phiAGO1. 3 to coexist in equilibrium with its host facilitates the selection of host mutants of attenuated virulence but does not preclude the phage antistaphylococcal activity in a nematode infection model. Front Microbiol 9:3227. https://doi.org/10.3389/fmicb.2018.03227

    Article  PubMed  PubMed Central  Google Scholar 

  44. Rakhuba DV, Kolomiets EI, Dey ES, Novik GI (2010) Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol 59(3):145–155

    Article  CAS  Google Scholar 

  45. Winstel V, Xia G, Peschel A (2014) Pathways and roles of wall teichoic acid glycosylation in Staphylococcus aureus. Int J Med Microbiol 304(3–4):215–221. https://doi.org/10.1016/j.ijmm.2013.10.009

    Article  CAS  PubMed  Google Scholar 

  46. Azam AH, Tanji Y (2019) Peculiarities of Staphylococcus aureus phages and their possible application in phage therapy. Appl Microbiol Biotechnol 103:4279–4289. https://doi.org/10.1007/s00253-019-09810-2

    Article  CAS  PubMed  Google Scholar 

  47. Koç C, Xia G, Kühner P, Spinelli S, Roussel A, Cambillau C, Stehle T (2016) Structure of the host-recognition device of Staphylococcus aureus phage ϕ11. Sci Rep 6(1):1–11. https://doi.org/10.1038/srep27581

    Article  CAS  Google Scholar 

  48. Takeuchi I, Osada K, Azam AH, Asakawa H, Miyanaga K, Tanji Y (2016) The presence of two receptor-binding proteins contributes to the wide host range of staphylococcal Twort-like phages. Appl Environ Microbiol 82(19):5763–5774. https://doi.org/10.1128/AEM.01385-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Cui Z, Guo X, Dong K, Zhang Y, Li Q, Zhu Y, Zeng L, Tang R, Li L (2017) Safety assessment of Staphylococcus phages of the family Myoviridae based on complete genome sequences. Sci Rep 7(1):1–8. https://doi.org/10.1038/srep41259

    Article  CAS  Google Scholar 

  50. Ajuebor J, Buttimer C, Arroyo-Moreno S, Chanishvili N, Gabriel EM, O’Mahony J, McAuliffe O, Neve H, Franz C, Coffey A (2018) Comparison of Staphylococcus phage K with close phage relatives commonly employed in phage therapeutics. Antibiotics 7(2):37. https://doi.org/10.3390/antibiotics7020037

    Article  CAS  PubMed Central  Google Scholar 

  51. Merabishvili M, Pirnay JP, Verbeken G, Chanishvili N, Tediashvili M, Lashkhi N, Glonti T, Krylov V, Mast J, Van Parys L, Lavigne R (2009) Quality-controlled small-scale production of a well-defined bacteriophage cocktail for use in human clinical trials. PLoS ONE 4(3):e4944. https://doi.org/10.1371/journal.pone.0004944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sulakvelidze A, Kutter E (2005) Bacteriophage therapy. In: Kutter E, Sulakvelidze A (eds) Bacteriophage biology and applications, 1st edn. CRC Press, Boca Raton, p 381–436

  53. Van Belleghem JD, Clement F, Merabishvili M, Lavigne R, Vaneechoutte M (2017) Pro- and anti-inflammatory responses of peripheral blood mononuclear cells induced by Staphylococcus aureus and Pseudomonas aeruginosa phages. Sci Rep 7(1):8004. https://doi.org/10.1038/s41598-017-08336-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Gutiérrez D, Fernández L, Rodríguez A, García P (2018) Are phage lytic proteins the secret weapon to kill Staphylococcus aureus? MBio 9(1):e01923-e2017. https://doi.org/10.1128/mBio.01923-17

    Article  PubMed  PubMed Central  Google Scholar 

  55. Adhya S, Merril CR, Biswas B (2014) Therapeutic and prophylactic applications of bacteriophage components in modern medicine. Cold Spring Harb Perspect Biol 4(1):a012518. https://doi.org/10.1101/cshperspect.a012518

    Article  CAS  Google Scholar 

  56. Schmelcher M, Shen Y, Nelson DC, Eugster MR, Eichenseher F, Hanke DC, Loessner MJ, Dong S, Pritchard DG, Lee JC, Becker SC (2015) Evolutionarily distinct bacteriophage endolysins featuring conserved peptidoglycan cleavage sites protect mice from MRSA infection. J Antimicrob Chemother 70(5):1453–1465. https://doi.org/10.1093/jac/dku552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Love MJ, Bhandari D, Dobson RC, Billington C (2018) Potential for bacteriophage endolysins to supplement or replace antibiotics in food production and clinical care. Antibiotics 7(1):17. https://doi.org/10.3390/antibiotics7010017

    Article  CAS  PubMed Central  Google Scholar 

  58. Becker SC, Roach DR, Chauhan VS, Shen Y, Foster-Frey J, Powell AM, Bauchan G, Lease RA, Mohammadi H, Harty WJ, Simmons C (2016) Triple-acting lytic enzyme treatment of drug-resistant and intracellular Staphylococcus aureus. Sci Rep 6(1):1–10. https://doi.org/10.1038/srep25063

    Article  CAS  Google Scholar 

  59. Becker SC, Swift S, Korobova O, Schischkova N, Kopylov P, Donovan DM, Abaev I (2015) Lytic activity of the staphylolytic Twort phage endolysin CHAP domain is enhanced by the SH3b cell wall binding domain. FEMS Microbiol Lett 362(1):1–8. https://doi.org/10.1093/femsle/fnu019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Sass P, Bierbaum G (2007) Lytic activity of recombinant bacteriophage φ11 and φ12 endolysins on whole cells and biofilms of Staphylococcus aureus. Appl Environ Microbiol 73(1):347–352. https://doi.org/10.1128/AEM.01616-06

    Article  CAS  PubMed  Google Scholar 

  61. Chang Y, Yoon H, Kang DH, Chang PS, Ryu S (2017) Endolysin LysSA97 is synergistic with carvacrol in controlling Staphylococcus aureus in foods. Int J Food Microbiol 244:19–26. https://doi.org/10.1016/j.ijfoodmicro.2016.12.007

    Article  CAS  PubMed  Google Scholar 

  62. Zhou Y, Zhang H, Bao H, Wang X, Wang R (2017) The lytic activity of recombinant phage lysin LysKΔamidase against staphylococcal strains associated with bovine and human infections in the Jiangsu province of China. Res Vet Sci 111:113–119. https://doi.org/10.1016/j.rvsc.2017.02.011

    Article  CAS  PubMed  Google Scholar 

  63. Obeso JM, Martínez B, Rodríguez A, García P (2008) Lytic activity of the recombinant staphylococcal bacteriophage ΦH5 endolysin active against Staphylococcus aureus in milk. Int J Food Microbiol 128(2):212–218. https://doi.org/10.1016/j.ijfoodmicro.2008.08.010

    Article  CAS  PubMed  Google Scholar 

  64. Fenton M, Keary R, McAuliffe O, Ross RP, O’Mahony J, Coffey A (2013) Bacteriophage-derived peptidase CHAP (K) eliminates and prevents Staphylococcal biofilms. Int J Microbiol 2013:625341. https://doi.org/10.1155/2013/625341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Schmelcher M, Powell AM, Becker SC, Camp MJ, Donovan DM (2012) Chimeric phage lysins act synergistically with lysostaphin to kill mastitis-causing Staphylococcus aureus in murine mammary glands. Appl Environ Microbiol 78(7):2297–2305. https://doi.org/10.1128/aem.07050-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Takáč M, Bläsi U (2005) Phage P68 virion-associated protein 17 displays activity against clinical isolates of Staphylococcus aureus. Antimicrob Agents Chemother 49(7):2934–2940. https://doi.org/10.1128/AAC.49.7.2934-2940.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Paul VD, Rajagopalan SS, Sundarrajan S, George SE, Asrani JY, Pillai R, Chikkamadaiah R, Durgaiah M, Sriram B, Padmanabhan S (2011) A novel bacteriophage Tail-Associated Muralytic Enzyme (TAME) from Phage K and its development into a potent antistaphylococcal protein. BMC Microbiol 11(1):1–11. https://doi.org/10.1186/1471-2180-11-226

    Article  CAS  Google Scholar 

  68. Liu J, Dehbi M, Moeck G, Arhin F, Bauda P, Bergeron D, Callejo M, Ferretti V, Ha N, Kwan T et al (2004) Antimicrobial drug discovery through bacteriophage genomics. Nat Biotechnol 22:185–191. https://doi.org/10.1038/nbt932

    Article  CAS  PubMed  Google Scholar 

  69. Kashani HH, Schmelcher M, Sabzalipoor H, Hosseini ES, Moniri R (2018) Recombinant endolysins as potential therapeutics against antibiotic-resistant Staphylococcus aureus: current status of research and novel delivery strategies. Clin Microbiol Rev 31(1):e00071-17. https://doi.org/10.1128/CMR.00071-17

    Article  Google Scholar 

  70. Dvořáčková M, Růžička F, Benešík M, Pantůček R, Dvořáková-Heroldová M (2019) Antimicrobial effect of commercial phage preparation Stafal® on biofilm and planktonic forms of methicillin-resistant Staphylococcus aureus. Folia Microbiol 64(1):121–126. https://doi.org/10.1007/s12223-018-0622-3

    Article  CAS  Google Scholar 

  71. Fischetti VA (2018) Development of phage lysins as novel therapeutics: a historical perspective. Viruses 10(6):310. https://doi.org/10.3390/v10060310

    Article  CAS  PubMed Central  Google Scholar 

  72. Patey O, McCallin S, Mazure H, Liddle M, Smithyman A, Dublanchet A (2019) Clinical indications and compassionate use of phage therapy: personal experience and literature review with a focus on osteoarticular infections. Viruses 11(1):18. https://doi.org/10.3390/v11010018

    Article  Google Scholar 

  73. Wittebole X, De Roock S, Opal SM (2014) A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 5(1):226–235. https://doi.org/10.4161/viru.25991

    Article  PubMed  Google Scholar 

  74. Tan SY, Tatsumura Y (2015) Alexander Fleming (1881–1955): discoverer of penicillin. Singapore Med J 56(7):366–367. https://doi.org/10.11622/smedj.2015105

    Article  PubMed  PubMed Central  Google Scholar 

  75. Lowy FD (2003) Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Investig 111(9):1265–1273. https://doi.org/10.1172/JCI18535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Abdelkader K, Gerstmans H, Saafan A, Dishisha T, Briers Y (2019) The preclinical and clinical progress of bacteriophages and their lytic enzymes: the parts are easier than the whole. Viruses 11(2):96. https://doi.org/10.3390/v11020096

    Article  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are thankful to Environmental Virology Cell, CSIR-NEERI, Nagpur and Director CSIR-NEERI for providing the research facility and infrastructure. Financial assistance to Akanksha Rai in form of fellowship from the University Grants Commission (UGC), India is gratefully acknowledged. We thank Traci Raley, MS, ELS, for editing a draft of this manuscript.

Funding

Financial assistance as fellowship from the University Grants Commission (UGC), India.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: Krishna Khairnar and Akanksha Rai; Writing and original draft preparation: Akanksha Rai; Writing, reviewing, and editing: Akanksha Rai and Krishna Khairnar.

Corresponding author

Correspondence to Krishna Khairnar.

Ethics declarations

Ethics approval

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Agnes M.S. Figueiredo

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rai, A., Khairnar, K. Overview of the risks of Staphylococcus aureus infections and their control by bacteriophages and bacteriophage-encoded products. Braz J Microbiol 52, 2031–2042 (2021). https://doi.org/10.1007/s42770-021-00566-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-021-00566-4

Keywords