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Control, Prevention and Rapid Detection of Methicillin-Resistant Staphylococcus aureus

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Bacteriophages: Practical Applications for Nature's Biocontrol

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) infections are a particular problem in hospitals . Wild phages can be reprogrammed for several clinical isolates of MRSA. These phages can then be utilized in a safe fogging biocontrol system, using specialized dispensers, along with another non toxic liquid variation as a surface disinfectant in healthcare or animal settings for the decontamination of MRSA and other antibiotic resistant bacteria. This phage-based biocontrol technology is non-toxic, odourless, inexpensive and effective in controlling and reducing the risk of contracting a hospital-acquired MRSA infection. By using phages as a biocontrol in medical facilities both staff and patients can feel safe from MRSA. This chapter will demonstrate the benefits of phage-based MRSA decontamination coupled with several rapid bacterial detection protocols enabling the development of inexpensive diagnostic kits and safe decontamination methods. There is also an urgent need for a real-time, accurate and inexpensive diagnostic kit that can be used in situ with no need for skilled technicians while also allowing patients to test for some diseases or conditions at home. These tests are cost-effective, quick, and confidential. The aim of this chapter is to provide a comprehensive overview of some innovative phage biocontrol methodologies and diagnostic kits that can be used in healthcare settings, while encouraging further research on the use of phages diagnostically and preventatively in daily decontamination practices.

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References

  • Abdalrahman LS, Wells H, Fakhr MK (2015) Staphylococcus aureus is more prevalent in retail beef livers than in pork and other beef cuts. Pathogens 4(2):182–198. doi:10.3390/pathogens4020182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abdulamir AS, Jassim SAA, Abu Bakar F (2014) Novel approach of using a cocktail of designed bacteriophages against gut pathogenic E. coli for bacterial load biocontrol. Ann Clin Microbiol Antimicrob 13:39. doi:10.1186/s12941-014-0039-z

  • Abdulamir AS, Jassim SAA, Hafidh RR, Bakar FA (2015) The potential of bacteriophage cocktail in eliminating Methicillin-resistant Staphylococcus aureus biofilms in terms of different extracellular matrices expressed by PIA, ciaA-D and FnBPA genes. Ann Clin Microbiol Antimicrob 14:49. doi:10.1186/s12941-015-0106-0. http://www.ncbi.nlm.nih.gov/pubmed/26558683

  • Abreu AC, Tavares RR, Anabela Borges A et al (2013) Current and emergent strategies for disinfection of hospital environments. J Antimicrob Chemother 68(12):2718–2732. doi:10.1093/jac/dkt281

    Article  CAS  PubMed  Google Scholar 

  • Aellen S, Que Y-A, Guignard B et al (2006) Detection of live and antibiotic-killed bacteria by quantitative real-time PCR of specific fragments of rRNA. Antimicrob Agents Chemother 50(6):1913–1920. doi:10.1128/AAC.00869-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aldoori AA, Mahdii EF, Abbas AK, Jassim SAA (2015) Bacteriophage biocontrol rescues mice bacteremic of clinically isolated mastitis from dairy cows associated with methicillin-resistant Staphyloccocus aureus. Adv Microbiol 5:383–403. doi:10.4236/aim.2015.56040

    Article  CAS  Google Scholar 

  • Alisky J, Iczkowski K, Rapoport A, Troitsky N (1998) Bacteriophages show promise as antimicrobial agents. J Infect 36(1):5–15

    Article  CAS  PubMed  Google Scholar 

  • Araki M, Kariyama R, Monden K et al (2002) Molecular epidemiological studies of Staphylococcus aureus in urinary tract infection. J Infect Chemother 8:168–174

    Article  CAS  PubMed  Google Scholar 

  • Argudín MÁ, Mendoza MC, Rodicio MR (2010) Food poisoning and Staphylococcus aureus enterotoxins. Toxins (Basel) 2(7):1751–1773. doi:10.3390/toxins2071751

    Article  CAS  Google Scholar 

  • Armand-Lefevre L, Ruimy R, Andremont A (2005) Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs. Emerg Infect Dis 11:711–714

    Article  PubMed  PubMed Central  Google Scholar 

  • Bachrach G, Leizerovici-Zigmond M, Zlotkin A et al (2003) Bacteriophage isolation from human saliva. Lett Appl Microbiol 36:50–53

    Article  PubMed  Google Scholar 

  • Bai J, Kim Y-T, Ryu S, Lee J-H (2016) Biocontrol and rapid detection of food-borne pathogens using bacteriophages and endolysins. Front Microbiol 7:article 474. doi:10.3389/fmicb.2016.00474

  • Baptiste K, Williams K, Willams N et al (2005) Methicillin-resistant staphylococci in companion animals. Emerg Infect Dis 11(12):1942–1944

    Article  PubMed  PubMed Central  Google Scholar 

  • Bentley DW, Bradley S, High K et al (2001) Practice guideline for evaluation of fever and infection in long-term care facilities. J Am Geriatr Soc 49:210–222

    Article  CAS  PubMed  Google Scholar 

  • Berendt AE, Turnbull L, Spady D et al (2011) Three swipes and you’re out: how many swipes are needed to decontaminate plastic with disposable wipes? Am J Infect Control 39(5):442–443. doi:10.1016/j.ajic.2010.08.014

    Article  PubMed  Google Scholar 

  • Bergeron M, Dauwalder O, Gouy M et al (2011) Species identification of staphylococci by amplification and sequencing of the tuf gene compared to the gap gene and by matrix-assisted laser desorption timeof-flight mass spectrometry. Eur J Clin Microbiol Infect Dis 30:343–354

    Article  CAS  PubMed  Google Scholar 

  • Bessonneau V, Clément M, Thomas O (2010) Can intensive use of alcohol-based hand rubs lead to passive alcoholization? Int J Environ Res Public Health 7(8):3038–3050. doi:10.3390/ijerph7083038

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhalla A, Aron DC, Donske CJ (2007) Staphylococcus aureus intestinal colonization is associated with increased frequency of S. aureus on skin of hospitalized patients. BMC Infect Dis 7:105. doi:10.1186/1471-2334-7-105

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhalla A, Pultz NJ, Gries DM et al (2004) Acquisition of nosocomial pathogens on hands after contact with environmental surfaces near hospitalized patients. Infect Control Hosp Epidemiol 25:164–167

    Article  PubMed  Google Scholar 

  • Bhargava K, Wang X, Donabedian S et al (2011) Methicillin-Resistant Staphylococcus aureus in Retail Meat, Detroit, Michigan, USA. Emerg Infect Dis 17(6):1135–1137. doi:10.3201/eid1706.101095

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhaskaran K, Hemalatha G, Sethumadhavan K (2014) Methicillin resistant Staphylococcus aureus carriage amongst students of the medical college. Int J Adv Res Biol Sci 1(7):188–192

    Google Scholar 

  • Blok HEM, Trolestra A, Kamp-Hopmans TEM et al (2003) Role of health care workers in outbreaks of methicillin resistant Staphylococcus aureus: a 10-year evaluation from a Dutch university hospital. Infect Control Hosp Epidemiol 24(9):679–685

    Google Scholar 

  • Blot S, Vandewoude K, Hoste E, Colardyn F (2002) Outcome and attributable mortality in critically Ill patients with bacteremia involving methicillin-susceptible and methicillin-resistant Staphylococcus aureus. Arch Intern Med 162:2229–2235

    Article  PubMed  Google Scholar 

  • Boost MV, O’Donoghue MM, James A (2008) Prevalence of Staphylococcus aureus carriage among dogs and their owners. Epidemiol Infect 136(7):953–964

    Article  CAS  PubMed  Google Scholar 

  • Boyce JM (2007) Environmental contamination makes an important contribution to hospital infection. J Hosp Infect 65(2):50–54. doi:10.1016/S0195-6701(07)60015-2

    Article  PubMed  Google Scholar 

  • Boyce JM, Havill NL (2005) Nosocomial antibiotic-associated diarrhea associated with enterotoxin-producing strains of methicillin-resistant Staphylococcus aureus. Am J Gastroenterol 100(8):1828–1834. doi:10.1111/j.1572-0241.2005.41510.x

    Article  PubMed  Google Scholar 

  • Boyce JM, Potter-Bynoe G, Chenevert C et al (1997) Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications. Infect Control Hosp Epidemiol 18(9):622–627

    Article  CAS  PubMed  Google Scholar 

  • Boyle-Vavra S, Daum RS (2007) Community acquired methicillin-resistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab Invest 87:3–9

    Article  CAS  PubMed  Google Scholar 

  • Brownlee C (2005) The Beef about UTIs. Food for thought. Biomedicine. Science News. 12 Jan 2005. https://www.sciencenews.org/blog/food-thought/beef-about-utis

  • Calfee DP, Salgado CD, Classen D et al (2008) Strategies to prevent transmission of methicillin-resistant Staphylococcus aureus in acute care hospitals. Infect Control Hosp Epidemiol 29(Suppl 1):S62–S80. doi:10.1086/591061

    Article  PubMed  Google Scholar 

  • Carling PC, Briggs JL, Perkins J, Highlander D (2006) Improved cleaning of patient rooms using a new targeting method. Clin Infect Dis 42(3):385–388

    Article  PubMed  Google Scholar 

  • Carling PC, Parry MF, Von Beheren SM (2008) Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals. Infect Control Hosp Epidemiol 29:1–7

    Article  CAS  PubMed  Google Scholar 

  • Carlton RM (1999) Phage therapy: past history and future prospects. Arch Immunol Ther Exp 47(5):267–274

    CAS  Google Scholar 

  • CDC (2007) MRSA: Methicillin-resistant Staphylococcus aureus in healthcare settings. Bulletin 14

    Google Scholar 

  • Chah KF, Gómez-Sanz E, Nwanta JA et al (2014) Methicillin-resistant coagulase-negative staphylococci from healthy dogs in Nsukka, Nigeria. Braz J Microbiol 45(1):215–220

    Article  PubMed  PubMed Central  Google Scholar 

  • Chua KY, Monk IR, Lin Y-H et al (2014) Hyperexpression of α-hemolysin explains enhanced virulence of sequence type 93 community-associated methicillin-resistant Staphylococcus aureus. BMC Microbiol 14:31. doi:10.1186/1471-2180-14-31

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Coll PP, Crabtree BF, O’Connor PJ, Klenzak S (1994) Clinical risk factors for methicillin-resistant Staphylococcus aureus bacteriuria in a skilled-care nursing home. Arch Fam Med 3:357–360

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove SE, Sakoulas G, Perencevich EN et al (2003) Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis 36:53–59

    Article  PubMed  Google Scholar 

  • Cosgrove SE, Qi Y, Kaye KS et al (2005) The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: mortality, length of stay, and hospital charges. Infect Control Hosp Epidemiol 26:166–174

    Article  PubMed  Google Scholar 

  • Cotterill S, Evans R, Fraise AP (1996) An unusual source for an outbreak of methicillin-resistant Staphylococcus aureus on an intensive therapy unit. J Hosp Infect 32:207–216

    Article  CAS  PubMed  Google Scholar 

  • Cui S, Li J, Hu C et al (2009) Isolation and characterization of methicillin-resistant Staphylococcus aureus from swine and workers in China. J Antimicrob Chemother 64:680–683

    Article  CAS  PubMed  Google Scholar 

  • Dancer SJ (2009) The role of environmental cleaning in the control of hospital-acquired infection. J Hosp Infect 73:378–385

    Article  CAS  PubMed  Google Scholar 

  • de Boer E, Zwartkruis-Nahuis JT, Wit B et al (2009) Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol 134:52–56. doi:10.1016/j.ijfoodmicro.2008.12.007

    Article  PubMed  CAS  Google Scholar 

  • de Neeling A, van den Broek M, Spalburg E et al (2007) High prevalence of methicillin resistant Staphylococcus aureus in pigs. Vet Microbiol 122:366–372

    Article  PubMed  CAS  Google Scholar 

  • de San Nour, Gasarira ODM-F, Mendonca RD et al (2007) Controlled evaluation of the IDI-MRSA assay for detection of colonization by methicillin-resistant Staphylococcus aureus in diverse musculocutaneous specimens. J Clin Microbiol 45:1098–1101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Denyer SP, Jassim SAA, Stewart GSAB (1991) In vivo bioluminescence for studying the adhesion of bacteria. Biofouling 5(issue 1–2):125–132

    Google Scholar 

  • Denyer SP, Jassim SAA, Fearon PS et al (1998) Genetically engineered reporter bacteria for the detection of bacteriophage. United States Patent 5723330. http://www.patentgenius.com/patent/5723330.html

  • Devriese LA, Van Damme LR, Famaree L (1972) Methicillin (cloxacillin) resistant Staphylococcus aureus strains isolated from bovine mastitis cases. Zentralbl Veterinarmed B 19:598–605

    Article  CAS  PubMed  Google Scholar 

  • Dewaele I, De Man I, Stael A et al (2008) Methicillin-resistant Staphylococcus aureus (MRSA) in Belgian pig farms. In: American Society for Microbiology (ASM) conference on antimicrobial resistance in zoonotic bacteria and foodborne pathogens, Copenhagen

    Google Scholar 

  • Diep BA, Otto M (2008) The role of virulence determinants in community-associated MRSA pathogenesis. Trends Microbiol 16:361–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle ME, Hartmann FA, Lee Wong AC (2012) Methicillin-resistant staphylococci: implications for our food supply? Anim Health Res Rev 13(2):157–180. doi:10.1017/S1466252312000187

    Article  PubMed  Google Scholar 

  • Drees M, Snydman DR, Schmid CH et al (2008) Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci. Clin Infect Dis 46:678–685

    Article  CAS  PubMed  Google Scholar 

  • Embleton ML, Nair SP, Heywood W et al (2005) Development of a novel targeting system for lethal photosensitization of antibiotic-resistant strains of Staphylococcus aureus. Antimicrob Agents Chemother 49(9):3690–3696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Enright MC, Robinson DA, Randle G et al (2002) The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). PNAS 99(11):7687–7692. doi:10.1073/pnas.122108599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fadeyi A, Adeboye MAN, Fowotade A et al (2010) Methicillin Resistant Staphylococcus aureus carriage amongst healthcare workers of the critical care units in a Nigerian hospital. Am J Infect Dis 6(1):18–23

    Article  Google Scholar 

  • Falagas ME, Thomaidis PC, Kotsantis IK et al (2011) Airborne hydrogen peroxide for disinfection of the hospital environment and infection control: a systematic review. J Hosp Infect 78:171–177

    Article  CAS  PubMed  Google Scholar 

  • Favrin SJ, Jassim SAA, Griffiths MW (2001) Development and optimization of a novel immunomagnetic separation—bacteriophage assay for the detection of Salmonella enterica Serovar enteritidis in broth. Appl Environ Microbiol 67(1):217–224. doi:10.1128/AEM.67.1.217-224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Favrin SJ, Jassim SAA, Griffiths MW (2003) Application of a novel immunomagnetic separation-bacteriophage assay for the detection of Salmonella enteritidis and Escherichia coli O157:H7 in food. Int J Food Microbiol 85(1–2):63–71. doi:10.1016/S0168-1605(02)00483-X

    Article  PubMed  Google Scholar 

  • Fenton M, Ross P, McAuliffe O et al (2010) Recombinant bacteriophage lysins as antibacterials. Bioeng Bugs 1(1):9–16

    Article  PubMed  PubMed Central  Google Scholar 

  • Fenton M, Keary R, McAuliffe O et al (2013) Bacteriophage-derived peptidase CHAPK eliminates and prevents staphylococcal Biofilms. Int J Microbiol 2013(ArticleI D625341):8. http://dx.doi.org/10.1155/2013/625341

  • Fischetti VA (2008) Bacteriophage lysins as effective antibacterials. Curr Opin Microbiol 11:393–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fitzgerald JR (2012) Human origin for livestock-associated methicillin-resistant Staphylococcus aureus. mBio 3(2):e00082-12. doi:10.1128/mBio.00082-12

  • Frank U (2003) Prevention and control of methicillin-resistant Staphylococcus aureus (MRSA). In: Fluit AC, Schmitz F-J (eds) MRSA current perspectives. Caister Academic Press, England. ch12, p 317–336. ISBN: 0-954264-5-4

    Google Scholar 

  • Garcia-Graells C, Antoine J, Larsen J et al (2012) Livestock veterinarians at high risk of acquiring methicillin-resistant Staphylococcus aureus ST398. Epidemiol Infect 140(03):383–389

    Article  CAS  PubMed  Google Scholar 

  • Goodman ER, Platt R, Bass R et al (2008) Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms. Infect Control Hosp Epidemiol 29(7):593–599

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodridge LD (2010) Designing phage therapeutics. Curr Pharm Biotechnol 11(1):15–27. doi:10.2174/138920110790725348

    Article  CAS  PubMed  Google Scholar 

  • Górski A, Borysowski J, Miedzybrodzki R, Weber-Dabrowska B (2007) Bacteriophages in medicine. In: McGrath S, van Sinderen D (eds) Bacteriophage: genetics and microbiology. Caister Academic Press, Norfolk, UK, pp 125–158

    Google Scholar 

  • Gorwitz RJ (2008) Understanding the success of methicillin-resistant Staphylococcus aureus strains causing epidemic disease in the community. J Infect Dis 197(2):179–182. doi:10.1086/523767

    Article  CAS  PubMed  Google Scholar 

  • Gould FK, Brindle R, Chadwick PR et al (2009) Guidelines (2008) for the prophylaxis and treatment of methicillin-resistant Staphylococcus aureus (MRSA) infections in the United Kingdom. J Antimicrob Chemother. doi:10.1093/jac/dkp065

    Google Scholar 

  • Graham P, Lin S, Larson E (2006) A U.S. population-based survey of Staphylococcus aureus colonization. Ann Intern Med 144:318–325

    Article  PubMed  Google Scholar 

  • Graveland H, Wagenaar JA, Broekhuizen-Stins MJ et al (2008) Methicillin-resistant Staphylococcus aureus (MRSA) in veal calf farmers and veal calves in the Netherlands. In: American Society for Microbiology (ASM) conference on antimicrobial resistance in zoonotic bacteria and foodborne pathogens, Copenhagen. pp 62–63

    Google Scholar 

  • Graveland H, Duim B, van Duijkeren E et al (2011a) Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int J Med Microbiol 301:630–634

    Article  PubMed  Google Scholar 

  • Graveland H, Wagenaar JA, Bergs K et al (2011b) Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS ONE 6:e16830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gravet A, Rondeau M, Harf-Monteil C et al (1999) Predominant Staphylococcus aureus isolated from antibiotic-associated diarrhea is clinically relevant and produces enterotoxin A and the bicomponent toxin LukE-lukD. J Clin Microbiol 37(12):4012–4019

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffeth GC, Morris DO, Abraham JL et al (2008) Screening for skin carriage of methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin. Vet Dermatol 19(3):142–149. doi:10.1111/j.1365-3164.2008.00663.x

    Article  PubMed  Google Scholar 

  • Griffith CJ, Cooper RA, Gilmore J et al (2000) An evaluation of hospital cleaning regimes and standards. J Hosp Infect 45(1):19–28

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez D, Ruas-Madiedo P, Martínez B et al (2014) Effective removal of Staphylococcal biofilms by the endolysin LysH5. PLoS ONE 9(9):e107307. doi:10.1371/journal.pone.0107307

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hallin M, Denis O, Deplano A et al (2008) Evolutionary relationships between sporadic and epidemic strains of healthcare-associated methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 14(7):659–669. doi:10.1111/j.1469-0691.2008.02015.x

    Article  CAS  PubMed  Google Scholar 

  • Hallin M, De Mendonça R, Denis O et al (2011) Diversity of accessory genome of human and livestock-associated ST398 methicillin resistant Staphylococcus aureus strains. Infect Genet Evol 11(2):290–299. doi:10.1016/j.meegid.2010.10.021

    Article  CAS  PubMed  Google Scholar 

  • Hanselman BA, Kruth SA, Rousseau J, Weese JS (2009) Coagulase positive staphylococcal colonization of humans and their household pets. Can Vet J 50:954–958

    PubMed  PubMed Central  Google Scholar 

  • Hanson BM, Dressler AE, Harper AL et al (2011) Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J Infect Public Health 4(4):169–174. doi:10.1016/j.jiph.2011.06.001

    Article  CAS  PubMed  Google Scholar 

  • Hasman H, Moodley A, Guardabassi L et al (2010) Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Vet Microbiol 141:326–331

    Article  CAS  PubMed  Google Scholar 

  • Hayden MK, Bonten MJ, Blom DW et al (2006) Reduction in acquisition of vancomycin-resistant Enterococcus after enforcement of routine environmental cleaning measures. Clin Infect Dis 42:1552–1560

    Article  PubMed  Google Scholar 

  • Hayden MK, Blom DW, Lyle EA (2008) Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant enterococcus or the colonized patients’ environment. Infect Control Hosp Epidemiol 29:149–154

    Article  PubMed  Google Scholar 

  • Hennekinne J-A, De Buyser M-L, Dragacci S (2012) Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev 36(4):815–836. doi:10.1111/j.1574-6976.2011.00311.x

    Article  CAS  PubMed  Google Scholar 

  • Hope CK, Packer S, Wilson M, Nair SP (2009) The inability of a bacteriophage to infect Staphylococcus aureus does not prevent it from specifically delivering a photosensitizer to the bacterium enabling its lethal photosensitization. J Antimicrob Chemother 64(1):59–61. doi:10.1093/jac/dkp157

    Article  CAS  PubMed  Google Scholar 

  • Huang SS, Datta R, Platt R (2006) Risk of acquiring antibiotic-resistant bacteria from prior room occupants. Arch Intern Med 166(18):1945–1951. doi:10.1001/archinte.166.18.1945

    Article  PubMed  Google Scholar 

  • Huber H, Koller S, Giezendanner N et al (2009) Methicillin-resistant Staphylococcus aureus (MRSA) in livestock animals and foods of animal origin in Switzerland. In: American Society for Microbiology (ASM)-ESCMID conference on methicillin-resistant Staphylococci in animals, London

    Google Scholar 

  • Huijsdens X, van Dijke B, Spalburg E et al (2006) Community acquired MRSA and pig-farming. Ann Clin Microbiol Antimicrob 5:26. doi:10.1186/1476-0711-5-26

    Article  PubMed  PubMed Central  Google Scholar 

  • Inamatsu T, Ooshima H, Masuda Y (1992) Clinical spectrum of antibiotic associated enterocolitis due to methicillin resistant Staphylococcus aureus. Nihon Rinsho 50(5):1087–1092

    CAS  PubMed  Google Scholar 

  • Institute for Healthcare Improvement (2014) Reducing MRSA infections: staying one step ahead. http://www.ihi.org/resources/Pages/ImprovementStories/ReducingMRSAInfectionsStayingOneStepAhead.aspx

  • Jain A, Agarwal J, Bansal S (2004) Prevalence of methicillin-resistant, coagulase-negative staphylococci in neonatal intensive care units: findings from a tertiary care hospital in India. J Med Microbiol 53:941–944. doi:10.1099/jmm.0.45565-0

    Article  PubMed  Google Scholar 

  • Jassim SAA (1989) Aspects of staphylococcal growth, haemolysis and phagocytosis. Ph.D. Thesis. University of Loughborough, UK. ASIN: B001A1RT34

    Google Scholar 

  • Jassim SAA, Griffiths MW (2007) Evaluation of a rapid microbial detection method via phage lytic amplification assay coupled with Live/Dead fluorochromic stains. Lett Appl Microbiol 44(6):673–678. doi:10.1111/j.1472-765X.2007.02115.x

  • Jassim SAA, Limoges RG (2014) Natural solution to antibiotic resistance: bacteriophages ‘The Living Drugs’. World J Microbiol Biotechnol 30(8):2153–2170. doi:10.1007/s11274-014-1655-7

    Article  PubMed  PubMed Central  Google Scholar 

  • Jassim SAA, Salt WG, Stretton RJ (1989) In vitro studies of haemolysis by some staphylococci grown in chemically defined media. J Appl Bacteriol 67(5):511–520

    Article  CAS  PubMed  Google Scholar 

  • Jassim SAA, Ellison A, Denyer SP, Stewart GSAB (1990) In vivo bioluminescence: a cellular reporter for research and industry. J Biolumin Chemilumin 5(2):115–122

    Article  CAS  PubMed  Google Scholar 

  • Jassim SAA, Akoush S, Griffiths MW (1996) Rapid detection using thermal change to monitor infection by host specific bacteriophage. IUFOST Meeting Food Associated Pathogens Uppsala, Sweden, May 1996

    Google Scholar 

  • Jassim SAA, Abdulamir AS, Abu Bakar F (2010a) Phage-based limulus amoebocyte lysate assay for rapid detection of bacteria. WO2011/098820A1. http://www.lens.org/images/patent/WO/2011098820/A1/WO_2011_098820_A1.pdf

  • Jassim SAA, Abdulamir AS, Abu Bakar F (2010b) Methods for bacteriophage design. WIPO Patent Application WO2010/064044 A1. http://www.sumobrain.com/patents/wipo/Methods-bacteriophage-design/WO2010064044A1.pdf

  • Jassim SAA, Abdulamir AS, Abu Bakar F (2012) Novel phage-based bio-processing of pathogenic Escherichia coli and its biofilms. World J Microbiol Biotechnol 28(1):47–60. doi:10.1007/s11274-011-0791-6

    Article  CAS  PubMed  Google Scholar 

  • Jevons MP (1961) Celbenin: resistant Staphylococci. Br Med J 1(5219):124–125

    Article  PubMed Central  Google Scholar 

  • Jończyk E, Kłak M, Międzybrodzki R, Górski A (2011) The influence of external factors on bacteriophages—review. Folia Microbiol 56(3):191–200. doi:10.1007/s12223-011-0039-8

    Article  CAS  Google Scholar 

  • Jones JW, Carter A, Ewings P, O’Boyle PJ (1999) An MRSA outbreak in a urology ward and its association with Nd:YAG coagulation laser treatment of the prostate. J Hosp Infect 41:39–44

    Article  CAS  PubMed  Google Scholar 

  • Jones TF, Kellum ME, Porter SS et al (2002) An outbreak of community-acquired foodborne illness caused by methicillin-resistant Staphylococcus aureus. Emerg Infect Dis 8:82–84

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson AP, Pearson A, Duckworth G (2005) Surveillance and epidemiology of MRSA bacteraemia in the UK. J Antimicrob Chemother 56:455–462

    Article  CAS  PubMed  Google Scholar 

  • Joshi SG, Paff M, Friedman G et al (2010) Control of methicillin-resistant Staphylococcus aureus in planktonic form and biofilms: a biocidal efficacy study of nonthermal dielectric-barrier discharge plasma. Am J Infect Control 38:293–301

    Article  CAS  PubMed  Google Scholar 

  • Juhász-Kaszanyitzky E, Jánosi S, Somogyi P et al (2007) MRSA transmission between cows and humans. Emerg Infect Dis 13(4):630–632

    Article  PubMed  PubMed Central  Google Scholar 

  • Kadariya J, Smith TC, Thapaliya D (2014) Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. BioMed Res Int 2014:827965. doi:10.1155/2014/827965

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaur S, Harjai K, Chhibber S (2012) Methicillin-resistant Staphylococcus aureus phage plaque size enhancement using sublethal concentrations of antibiotics. Appl Environ Microbiol 78(23):8227–8233. doi:10.1128/AEM.02371-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaźmierczak Z, Górski A, Dąbrowska K (2014) Facing antibiotic resistance: Staphylococcus aureus phages as a medical tool. Viruses 6:2551–2570. doi:10.3390/v6072551

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kelly D, McAuliffe O, Ross RP, Coffey A (2012) Prevention of Staphylococcus aureus biofilm formation and reduction in established biofilm density using combination of phage K and modified derivatives. Lett Appl Microbiol 54(4):286–291

    Article  CAS  PubMed  Google Scholar 

  • Khanna T, Friendship R, Dewey C, Weese JS (2007) Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet Microbiol 128:298–303

    Article  PubMed  CAS  Google Scholar 

  • Klein E, Smith DL, Laxminarayan R (2007) Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999–2005. Emerg Infect Dis 13:1840–1846

    Article  PubMed  PubMed Central  Google Scholar 

  • Klevens RM, Morrison MA, Nadle J et al (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298:1763–1771

    Article  CAS  PubMed  Google Scholar 

  • Kluytmans J, van Leeuwen W, Goessens W et al (1995) Food-initiated outbreak of methicillin-resistant Staphylococcus aureus analyzed by pheno- and genotyping. J Clin Microbiol 33:1121–1128

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knudsen AM, Rosdahl VT (1991) The decline of methicillin resistance among Danish Staphylococcus aureus strains. Infect Control Hosp Epidemiol 12:83–88

    Article  PubMed  Google Scholar 

  • Köck R, Becker K, Cookson B et al (2010) Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. Euro Surveill 15(41):19688. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19688A

  • Köck R, Schaumburg F, Mellmann A et al (2013) Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection and colonization in Germany. PLoS ONE 8(2):e55040. doi:10.1371/journal.pone.0055040

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kodama T, Santo T, Yokoyama T et al (1997) Postoperative enteritis caused by methicillin-resistant Staphylococcus aureus. Surg Today 27(9):816–825. doi:10.1007/BF02385272

    Article  CAS  PubMed  Google Scholar 

  • Kramer A, Kampf G (2007) Hand rub-associated fire incidents during 25038 hospital-years in Germany. Infect Control Hosp Epidemiol 28(6):745–746

    Article  PubMed  Google Scholar 

  • Kramer A, Schwebke I, Kampf G (2006) How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis 6:130. doi:10.1186/1471-2334-6-130

    Article  PubMed  PubMed Central  Google Scholar 

  • Krylov VN (2001) Phagotherapy in terms of bacteriophage genetics: hopes, perspectives, safety, limitations. Genetika 37(7):869–887

    CAS  PubMed  Google Scholar 

  • Kumar P, Shukla I, Varshney S (2011) Nasal screening of healthcare workers for nasal carriage of coagulase positive MRSA and prevalence of nasal colonization with Staphylococcus aureus. Biol Med 27(1):62–64

    Google Scholar 

  • Kutateladze M, Adamia R (2010) Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol 28(12):591–595

    Article  CAS  PubMed  Google Scholar 

  • Kutter E, De Vos D, Gvasalia G et al (2010) Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol 11(1):69–86

    Article  CAS  PubMed  Google Scholar 

  • Kwon NH, Park KT, Moon JS et al (2005) Staphylococcal cassette chromosome MEC (SCCMEC) characterization and molecular analysis for methicillin-resistant Staphylococcus aureus and novel SCCMEC subtype IVG isolated from bovine milk in Korea. J Antimicrob Chemother 56:624–632

    Article  CAS  PubMed  Google Scholar 

  • Labandeira-Rey M, Couzon F, Boisset S et al (2007) Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315(5815):1130–1135. doi:10.1126/science.1137165

    Article  CAS  PubMed  Google Scholar 

  • Lee J (2003) Methicillin (oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Appl Environ Microbiol 69:6489–6494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J (2006) Occurrence of methicillin-resistant Staphylococcus aureus strains from cattle and chicken, and analyses of their mecA, mecR1 and mecI genes. Vet Microbiol 114:155–159

    Article  CAS  PubMed  Google Scholar 

  • Lehner G, Linek M, Bond R et al (2014) Case-control risk factor study of methicillin-resistant Staphylococcus pseudintermedius (MRSP) infection in dogs and cats in Germany. Vet Microbiol 168(1):154–160. doi:10.1016/j.vetmic.2013.10.023

    Article  PubMed  Google Scholar 

  • Leonard F, Abbott Y, Rossney A et al (2006) Methicillin-resistant Staphylococcus aureus isolated from a veterinary surgeon and five dogs in one practice. Vet Rec 158(5):155–159

    Article  CAS  PubMed  Google Scholar 

  • Lim SK, Nam HM, Park HJ et al (2010) Prevalence and characterization of methicillin-resistant Staphylococcus aureus in raw meat in Korea. J Microbiol Biotechnol 20:775–778

    CAS  PubMed  Google Scholar 

  • Lin J, Yeh KS, Liu HT, Lin JH (2009) Staphylococcus aureus isolated from pork and chicken carcasses in Taiwan: prevalence and antimicrobial susceptibility. J Food Prot 72:608–611

    Article  CAS  PubMed  Google Scholar 

  • Lopez P-J, Ron O, Parthasarathy P et al (2009) Bacterial counts from hospital doctors’ ties are higher than those from shirts. Am J Infect Control 37:79–80

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lozano C, López M, Gómez-Sanz E et al (2009) Detection of methicillin-resistant Staphylococcus aureus ST398 in food samples of animal origin in Spain. J Antimicrob Chemother 64:1325–1326

    Article  CAS  PubMed  Google Scholar 

  • Ma XX, Sun DD, Wang S et al (2011) Nasal carriage of methicillin-resistant Staphylococcus aureus among preclinical medical students: epidemiologic and molecular characteristics of methicillin-resistant S. aureus clones. Diagn Microbiol Infect Dis 70:22–30

    Article  CAS  PubMed  Google Scholar 

  • Malhotra-Kumar S, Haccuria K, Michiels M et al (2008) Current trends in rapid diagnostics for methicillin-resistant Staphylococcus aureus and glycopeptide-resistant enterococcus species. J Clin Microbiol 46(5):1577–1587. doi:10.1128/JCM.00326-08

    Article  PubMed  PubMed Central  Google Scholar 

  • Malik RE, Cooper RA, Griffith CJ (2003) Use of audit tools to evaluate the efficacy of cleaning systems in hospitals. Am J Infect Control 31(3):181–187

    Article  PubMed  Google Scholar 

  • Malik S, Peng H, Barton MD (2005) Antibiotic resistance in staphylococci associated with cats and dogs. J Appl Microbiol 99(6):1283–1293

    Article  CAS  PubMed  Google Scholar 

  • Marler B (2010) About MRSA (Methicillin-resistant Staphylococcus aureus). Food Poison J. http://www.foodpoisonjournal.com/food-poisoning-information/about-mrsa-methicillinresistant-staphylococcus-aureus/

  • Martinez JA, Ruthazer R, Hansjosten K et al (2003) Role of environmental contamination as a risk factor for acquisition of vancomycin-resistant Enterococci in patients treated in a medical intensive care unit. Arch Intern Med 163(16):1905–1912

    Article  PubMed  Google Scholar 

  • May L, Klein EY, Rothman RE, Laxminarayanc R (2014) Trends in antibiotic resistance in coagulase-negative staphylococci in the United States, 1999 to 2012. Antimicrob Agents Chemother 58(3):1404–1409

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McAnoy AM (2006) Vaporous decontamination methods: potential uses and research priorities for chemical and biological contamination control. Report number: DSTO-GD-0465. Publisher Human Protection and Performance Division, DSTO Defence Science and Technology Organisation, Commonwealth of Australia. http://dspace.dsto.defence.gov.au/dspace/handle/1947/3415

  • McCarthy AJ, Witney AA, Gould KA et al (2011) The distribution of mobile genetic elements (MGEs) in MRSA CC398 is associated with both host and country. Genome Biol Evol 3:1164–1174. doi:10.1093/gbe/evr092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McIntyre L, Jassim SAA, Griffiths MW (1996) Development of a bacteriophage-mediated ATP bioluminescence detection system for Listeria monocytogenes. Presented at 83rd Annual Meeting of IAMFES, Seattle, WA, June 30–July 3, 1996, p 70

    Google Scholar 

  • McNamee PT, Smyth JA (2000) Bacterial chondronecrosis with osteomyelitis (femoral head necrosis) of broiler chickens. Avian Pathol 29:253–270. doi:10.1080/030794500750047243

    Article  CAS  PubMed  Google Scholar 

  • MDH (Minnesota Department of Health) (2004) Community-associated methicillin resistant Staphylococcus aureus in Minnesota. Dis Control News 32:61–72

    Google Scholar 

  • Moodley A, Damborg P, Nielsen SS (2014) Antimicrobial resistance in methicillin susceptible and methicillin resistant Staphylococcus pseudintermedius of canine origin: literature review from 1980 to 2013. Vet Microbiol 171(3–4):337–341. doi:10.1016/j.vetmic.2014.02.008

    Article  CAS  PubMed  Google Scholar 

  • Moon JS, Lee AR, Kang HM et al (2007) Phenotypic and genetic antibiogram of methicillin resistant staphylococci isolated from bovine mastitis in Korea. J Dairy Sci 90(3):1176–1185

    Article  CAS  PubMed  Google Scholar 

  • Moran GJ, Krishnadasan A, Gorwitz RJ et al (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med 355(7):666–674

    Article  CAS  PubMed  Google Scholar 

  • Morgan DJ, Rogawski E, Thom KA et al (2012) Transfer of multidrug-resistant bacteria to healthcare workers’ gloves and gowns after patient contact increases with environmental contamination. Crit Care Med 40(4):1045–1051. doi:10.1097/CCM.0b013e31823bc7c8

    Article  PubMed  PubMed Central  Google Scholar 

  • Morioka I, Takahashi N, Kitajima H (2014) Prevalence of MRSA colonization in Japanese neonatal care unit patients in 2011. Pediatr Int 56(2):211–214. doi:10.1111/ped.12232

    Article  PubMed  Google Scholar 

  • Morris D, Mauldin E, O’Shea K et al (2006) Clinical, microbiological, and molecular characterization of methicillin-resistant Staphylococcus aureus infections of cats. Am J Vet Res 67(8):1421–1425

    Article  CAS  PubMed  Google Scholar 

  • Muder RR, Brennen C, Rihs JD et al (2006) Isolation of Staphylococcus aureus from the urinary tract: association of isolation with symptomatic urinary tract infection and subsequent staphylococcal bacteremia. Clin Infect Dis 42(1):46–50. doi:10.1086/498518

    Article  PubMed  Google Scholar 

  • Muto CA, Jernigan JA, Ostrowsky BE et al (2003) SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infect Control Hosp Epidemiol 24(5):362–386

    Article  PubMed  Google Scholar 

  • Mylotte JM, Tayara A, Goodnough S (2002) Epidemiology of bloodstream infection in nursing home residents: evaluation in a large cohort from multiple homes. Clin Infect Dis 35:1484–1490

    Article  PubMed  Google Scholar 

  • Nakamura S, Yang CS, Sakon N et al (2009) Direct metagenomic detection of viral pathogens in nasal and fecal specimens using an unbiased high-throughput sequencing approach. PLoS ONE 4:e4219

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nemati M, Hermans K, Lipinska U et al (2008) Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrob Agents Chemother 52:3817–3819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nienhoff U, Kadlec K, Chaberny IF et al (2009) Transmission of methicillin-resistant Staphylococcus aureus strains between humans and dogs: two case reports. J Antimicrob Chemother 64(3):660–662

    Article  CAS  PubMed  Google Scholar 

  • Ogawa Y, Saraya T, Koide T et al (2014) Methicillin-resistant Staphylococcus aureus enterocolitis sequentially complicated with septic arthritis: a case report and review of the literature. BMC Res Notes 7:21. doi:10.1186/1756-0500-7-21

    Article  PubMed  PubMed Central  Google Scholar 

  • Okuyama Y, Yoshida N (2012) Staphylococcal food poisoning and MRSA enterocolitis. Nihon Rinsho 70(8):1362–1365

    PubMed  Google Scholar 

  • Noskin GA, Rubin RJ, Schentag JJ et al (2005) The burden of Staphylococcus aureus infections on hospitals in the United States: an analysis of the 2000 and 2001 nationwide inpatient sample database. Arch Intern Med 165:1756–1761

    Article  PubMed  Google Scholar 

  • O’Flaherty S, Ross RP, Meaney W et al (2005) Potential of the polyvalent anti-Staphylococcus bacteriophage K for control of antibiotic-resistant staphylococci from hospitals. App environ microbiol 71:1836–1842. doi:10.1128/AEM.71.4.1836-1842.2005

    Article  CAS  Google Scholar 

  • Olson M, Ceri H, Morck D et al (2002) Biofilm bacteria: formation and comparative susceptibility to antibiotics. Can J Vet Res 66:86–92

    PubMed  PubMed Central  Google Scholar 

  • Otter JA, Vickery K, Walker JT et al (2014) Surface-attached cells, biofilms and biocide susceptibility: implications for hospital cleaning and disinfection. J Hosp Infect. doi:10.1016/j.jhin.2014.09.008

    Google Scholar 

  • Pacio GA, Visintainer P, Maguire G et al (2003) Natural history of colonization with vancomycin-resistant enterococci, methicillin-resistant Staphylococcus aureus, and resistant gram-negative bacilli among ling-term-care facility residents. Infect Control Hosp Epidemiol 24:246–250

    Article  PubMed  Google Scholar 

  • Page K, Wilson M, Parkin IP (2009) Antimicrobial surfaces and their potential in reducing the role of the inanimate environment in the incidence of hospital-acquired infections. J Mater Chem 19:3819–3831. doi:10.1039/B818698G

    Article  CAS  Google Scholar 

  • Palavecino E (2004) Community-acquired methicillin-resistant Staphylococcus aureus infections. Clin Lab Med 24(2):403–418

    Article  PubMed  Google Scholar 

  • Palavecino EL (2014) Clinical, epidemiologic, and laboratory aspects of methicillin-resistant Staphylococcus aureus infections. Meth mol boil 1085:1–24

    Article  CAS  Google Scholar 

  • Pastagia M, Euler C, Chahales P et al (2011) A novel chimeric lysin shows superiority to mupirocin for skin decolonization of methicillin-resistant and -sensitive Staphylococcus aureus strains. Antimicrob Agents Chemother 55:738–744

    Article  CAS  PubMed  Google Scholar 

  • Pereira V, Lopes C, Castro A et al (2009) Characterization for enterotoxin production, virulence factors, and antibiotic susceptibility of Staphylococcus aureus isolates from various foods in Portugal. Food Microbiol 26(3):278–282

    Article  CAS  PubMed  Google Scholar 

  • Persoons D, Van Hoorebeke S, Hermans K et al (2009) Methicillin-resistant Staphylococcus aureus in poultry. Emerging Infect Dis 15:452–453

    Article  PubMed  PubMed Central  Google Scholar 

  • Peters PJ, Brooks JT, McAllister SK et al (2013) Methicillin-resistant Staphylococcus aureus colonization of the groin and risk for clinical infection among HIV-infected adults. Emerg Infect Dis 19(4):623–629. doi:10.3201/eid1904.121353

    Article  PubMed  PubMed Central  Google Scholar 

  • Price LB, Steggerb M, Hasman H et al (2012) Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3(1):e00305-11

    Google Scholar 

  • Pu S, Han F, Ge B (2009) Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl Environ Microbiol 75:265–267. doi:10.1128/AEM.01110-08

    Article  CAS  PubMed  Google Scholar 

  • Rashel M, Uchiyama J, Ujihara T et al (2007) Efficient elimination of multidrug-resistant Staphylococcus aureus by cloned lysin derived from bacteriophage phi MR11. J Infect Dis 196(8):1237–1247

    Article  CAS  PubMed  Google Scholar 

  • Rasigade JP, Laurent F, Hubert P et al (2010) Lethal necrotizing pneumonia caused by an ST398 Staphylococcus aureus strain. Emerg Infect Dis 16(8):1330. doi:10.3201/eid1608.100317

    Article  PubMed  PubMed Central  Google Scholar 

  • Rastogi V, Pragya, Verma N et al (2016) An overview on bacteriophages: a natural nanostructured antibacterial agent. Curr Drug Deliv 13(8) (E-pub ahead of print)

    Google Scholar 

  • Ray AJ, Pultz NJ, Bhalla A et al (2003) Coexistence of vancomycin-resistant enterococci and Staphylococcus aureus in the intestinal tracts of hospitalized patients. Clin Infect Dis 37:875–881. doi:10.1086/377451

    Article  PubMed  Google Scholar 

  • Rubin JE, Gaunt MC (2011) Urinary tract infection caused by methicillin-resistant Staphylococcus pseudintermedius in a dog. Can Vet J 52(2):162–164

    PubMed  PubMed Central  Google Scholar 

  • Sass P, Bierbaum G (2007) Lytic activity of recombinant bacteriophage 11 and 12 endolysins on whole cells and biofilms of Staphylococcus aureus. Appl Environ Microbiol 73(1):347–352

    Article  CAS  PubMed  Google Scholar 

  • Schmelcher M, Loessner MJ (2016) Bacteriophage endolysins: applications for food safety. Curr Opin Biotechnol 37:76–87. doi:10.1016/j.copbio.2015.10.005

    Article  CAS  PubMed  Google Scholar 

  • Seaman A (2013) Hospital-acquired MRSA infection rates falling: CDC, Reuters. http://www.reuters.com/article/us-hospital-mrsa-idUSBRE98F0X920130916

  • Sergio D, Koh T, Hsu L et al (2007) Investigation of methicillin-resistant Staphylococcus aureus in pigs used for research. J Med Microbiol 56:1107–1109

    Article  PubMed  Google Scholar 

  • Schelin J, Wallin-Carlquist N, Thorup Cohn M et al (2011) The formation of Staphylococcus aureus enterotoxin in food environments and advances in risk assessment. Virulence 2(6):580–592. doi:10.4161/viru.2.6.18122

    Article  PubMed  PubMed Central  Google Scholar 

  • Schentag JJ, Hyatt J, Carr J (1998) Genesis of methicillin-resistant Staphylococcus aureus (MRSA). How treatment of MRSA infections has selected for vancomycin-resistant Enterococcus faecium and the importance of antibiotic management and infection control. Clin Infect Dis 26:1204–1214

    Article  CAS  PubMed  Google Scholar 

  • Schijffelen MJ, Boel CH, van Strijp JA, Fluit AC (2010) Whole genome analysis of a livestock-associated methicillin-resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis. BMC Genom 11:376. doi:10.1186/1471-2164-11-376

    Article  CAS  Google Scholar 

  • Schwarz S, Kadlec K, Strommenger B (2007) Methicillin-resistant Staphylococcus aureus and staphylococcus pseudintermedius detected in the BFT-germvet monitoring programme 2004-2006 in Germany. J Antimicrob Chemother 61:282–285

    Article  PubMed  CAS  Google Scholar 

  • Shepheard MA, Fleming VM, Connor TR et al (2013) Historical zoonoses and other changes in host tropism of Staphylococcus aureus, identified by phylogenetic analysis of a population dataset. PLoS ONE 8:e62369. doi:10.1371/journal.pone.0062369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shlaes DM, Gerding DN, John JF (1997) Society for healthcare epidemiology of America and infectious diseases society of America joint committee on the prevention of antimicrobial resistance: guidelines for the prevention of antimicrobial resistance in hospitals. Infect Control Hosp Epidemiol 18:275–2791

    Article  CAS  PubMed  Google Scholar 

  • Siegel JD, Rhinehart E, Jackson M et al (2007) Management of multidrug-resistant organisms in health care settings, 2006. Am J Infect Control 35(10 Suppl 2):S165–S193

    Google Scholar 

  • Simões M, Simões LC, Vieira MJ (2010) A review of current and emergent biofilm control strategies. Food Sci Technol 43(4):573–583

    Google Scholar 

  • Simpson WJ, Fernandez JL, Hammond JRM et al (1990) A Highly sensitive assay for adenosine triphosphate employing an improved firefly luciferase reagent. Lett Appl Microbiol 11(4):208–210. doi:10.1111/j.1472-765X.1990.tb00162.x

    Article  CAS  Google Scholar 

  • Smith TC, Male MJ, Harper AL et al (2008a) Isolation of methicillin-resistant Staphylococcus aureus (MRSA) from swine in the midwestern United States. In: International conference on emerging infectious diseases, Atlanta

    Google Scholar 

  • Smith TC, Male MJ, Harper AL et al (2008b) Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in Midwestern US swine and swine workers. PLoS ONE 4:e4258

    Article  PubMed  Google Scholar 

  • Soejima T, Iida K, Qin T et al (2008) Method to detect only live bacteria during PCR amplification. J Clin Microbiol 46(7):2305–2313. doi:10.1128/JCM.02171-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Son JS, Lee SJ, Jun SY et al (2010) Antibacterial and biofilm removal activity of a podoviridae Staphylococcus aureus bacteriophage SAP-2 and a derived recombinant cell-wall-degrading enzyme. Appl Microbiol Biotechnol 86(5):1439–1449

    Article  CAS  PubMed  Google Scholar 

  • Squier C, Rihs JD, Risa KJ et al (2002) 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. doi:10.1086/502095

    Article  PubMed  Google Scholar 

  • Stewart GSAB, Jassim SAA, Denyer SP et al (1998) The specific and sensitive detection of bacterial pathogens within 4 h using bacteriophage amplification. J Appl Bacteriol 84(5):777–783. doi:10.1046/j.1365-2672.1998.00408.x

  • Stürenburg E (2009) Rapid detection of methicillin-resistant Staphylococcus aureus directly from clinical samples: methods, effectiveness and cost considerations. Ger Med Sci 7:Doc06. doi:10.3205/000065

  • Tacconelli E, De Angelis G, Cataldo MA et al (2008) Does antibiotic exposure increase the risk of methicillin-resistant Staphylococcus aureus (MRSA) isolation? A systematic review and meta-analysis. J Antimicrob Chemother 61:26–38

    Article  CAS  PubMed  Google Scholar 

  • Takesue Y, Yokoyama T, Kodama T et al (1991) Toxin involvement in methicillin-resistant Staphylococcus aureus enteritis in gastroenterological surgery. Gastroenterol Jpn 26(6):716–720

    CAS  PubMed  Google Scholar 

  • Talon D (1999) The role of the hospital environment in the epidemiology of multi-resistant bacteria. J Hosp Infect 43:13–17

    Article  CAS  PubMed  Google Scholar 

  • Ternes YM, Lamaro-Cardoso J, André MCP et al (2013) Molecular epidemiology of coagulase-negative Staphylococcus carriage in neonates admitted to an intensive care unit in Brazil. BMC Infect Dis 13:572. doi:10.1186/1471-2334-13-572

    Article  PubMed  PubMed Central  Google Scholar 

  • Tomlin J, Pead MJ, Lloyd DH et al (1999) Methicillin-resistant Staphylococcus aureus infections in 11 dogs. Vet Rec 144(3):60–64. doi:10.1136/vr.144.3.60

    Article  CAS  PubMed  Google Scholar 

  • Toté K, Berghe DV, Deschacht M et al (2009) Inhibitory efficacy of various antibiotics on matrix and viable mass of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Int J Antimicrob Agents 33:525–531

    Article  PubMed  CAS  Google Scholar 

  • USDA-FSIS (2014) Pre-harvest management controls and intervention options for reducing Shiga toxin-producing Escherichia coli shedding in cattle: an overview of current research. http://www.fsis.usda.gov/wps/wcm/connect/d5314cc7-1ef7-4586-bca2-f2ed86d9532f/Reducing-Ecoli-Shedding-in-Cattle.pdf?MOD=AJPERES

  • van Cleef BA, Graveland H, Haenen APJ 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(3):1030–1033. doi:10.1128/JCM.00493-10

    Article  PubMed  PubMed Central  Google Scholar 

  • van der Mee-Marquet N, François P, Domelier-Valentin AS et al (2011) Emergence of unusual bloodstream infections associated with pig-borne-like Staphylococcus aureus ST398 in France. Clin Infect Dis 52(1):152–153. doi:10.1093/cid/ciq053

    Article  PubMed  Google Scholar 

  • van Duijkeren E, Jansen MD, Flemming SC et al (2007) Methicillin-resistant Staphylococcus aureus in pigs with exudative epidermitis. Emerging Infect Dis 13:1408–1410

    Article  PubMed  PubMed Central  Google Scholar 

  • van Duijkeren E, Ikawaty R, Broekhuizen-Stins M et al (2008) Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Vet Microbiol 126:383–389

    Article  PubMed  Google Scholar 

  • van Duijkeren E, Moleman M, Sloet van Oldruitenborgh-Oosterbaan MM et al (2010) Methicillin-resistant Staphylococcus aureus in horses and horse personnel: an investigation of several outbreaks. Vet Microbiol 141(1–2):96–102. doi:10.1016/j.vetmic.2009.08.009

    Article  PubMed  Google Scholar 

  • van Loo IH, Diederen BM, Savelkoul PH et al (2007) Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands. Emerging Infect Dis 13:1753–1755

    Article  PubMed  PubMed Central  Google Scholar 

  • Vandenesch F, Naimi T, Enright MC et al (2003) Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9:978–984

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanderhaeghen W, Hermans K, Haesebrouck F, Butaye P (2010) Methicillin-resistant Staphylococcus aureus (MRSA) in food production animals. Epidemiol Infect 138(5):606–625. doi:10.1017/S0950268809991567

    Article  CAS  PubMed  Google Scholar 

  • Verasa JF, do Carmob LS, Tongc LC et al (2008) A study of the enterotoxigenicity of coagulase-negative and coagulase-positive staphylococcal isolates from food poisoning outbreaks in Minas Gerais, Brazil. Int J Infect Dis 12(4):410–415

    Google Scholar 

  • Viana D, Selva L, Segura P et al (2007) Genotypic characterization of Staphylococcus aureus strains isolated from rabbit lesions. Vet Microbiol 121:288–298. doi:10.1016/j.vetmic.2006.12.003

    Article  CAS  PubMed  Google Scholar 

  • Viertel TM, Ritter K, Horz H-P (2014) Viruses versus bacteria—novel approaches to phage therapy as a tool against multidrug-resistant pathogens. J Antimicrob Chemother 69(9):2326–2336. doi:10.1093/jac/dku173

    Article  CAS  PubMed  Google Scholar 

  • Vitale CB, Gross TL, Weese JS (2006) Methicillin-resistant Staphylococcus aureus in cat and owner. Emerging Infect Dis 12(12):1998–2000. doi:10.3201/eid1212.060725

    Article  PubMed  PubMed Central  Google Scholar 

  • Von Eiff C, Arciola CR, Montanaro L et al (2006) Emerging Staphylococcus species as new pathogens in implant infections. Int J Artific Organs 29:360–367

    Google Scholar 

  • Voss A, Loeffen F, Bakker J et al (2005) Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect Dis 11:1965–1966

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagenaar JA, Yue H, Pritchard J et al (2009) Unexpected sequence types in livestock associated methicillin-resistant Staphylococcus aureus (MRSA): MRSA ST9 and a single locus variant of ST9 in pig farming in China. Vet Microbiol 139:405–409

    Article  CAS  PubMed  Google Scholar 

  • Walker A, Jassim SAA, Holah JT et al (1992) Bioluminescent Listeria monocytogenes provide a rapid assay for measuring biocide efficacy. FEMS Microbiol Lett 91(Issue 3):251–255

    Google Scholar 

  • Wang R, Braughton KR, Kretschmer D et al (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13(12):1510–1514

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Li Y, Mustapha A (2009) Detection of viable Escherichia coli O157:H7 by ethidium monoazide real-time PCR. J Appl Microbiol 107(5):1719–1728. doi:10.1111/j.1365-2672.2009.04358.x

    Article  CAS  PubMed  Google Scholar 

  • Weber DJ, Rutala WA, Miller MB et al (2010) Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species. Am J Infect Control 38(Suppl 1):S25–S33

    Article  PubMed  Google Scholar 

  • Weese JS (2010) Methicillin-resistant Staphylococcus aureus in animals. ILAR J 51:233–244. doi:10.1093/ilar.51.3.233

    Article  CAS  PubMed  Google Scholar 

  • Weese JS, Avery BP, Gow S (2009a) Methicillin-resistant Staphylococcus aureus (MRSA) surveillance in slaughter-age pigs and feedlot cattle. In: American Society for Microbiology (ASM)-ESCMID conference on methicillin-resistant staphylococci in animals, London

    Google Scholar 

  • Weese JS, Avery B, Rousseau J, Reid-Smith R (2009b) Methicillin-resistant Staphylococcus aureus contamination of retail meat: Canada. In: American Society for Microbiology (ASM)-ESCMID conference on methicillin resistant staphylococci in animals, London

    Google Scholar 

  • Weese JS, Avery BP, Reid-Smith RJ (2010) Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products. Lett Appl Microbiol 51:338–342. doi:10.1111/j.1472-765X.2010.02901.x

    Article  CAS  PubMed  Google Scholar 

  • Weese JS, Dick H, Willey BM et al (2006) Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Vet Microbiol 115(1–3):148–155

    Article  CAS  PubMed  Google Scholar 

  • Weese JS, Sweetman K, Edson H, Rousseau J (2013) Evaluation of minocycline susceptibility of methicillin-resistant Staphylococcus pseudintermedius. Vet Microbiol 162(2–4):968–971. doi:10.1016/j.vetmic.2012.10.002

    Article  CAS  PubMed  Google Scholar 

  • Wendlandt S, Schwarz S, Silley P (2013) Methicillin-resistant Staphylococcus aureus: a food-borne pathogen? Annu Rev Food Sci Technol 4:117–139. doi:10.1146/annurev-food-030212-182653

    Article  CAS  PubMed  Google Scholar 

  • Witte W, Strommenger B, Stanek C, Cuny C (2007) Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, central Europe. Emerging Infect Dis 13(12):255–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whiteley GS, Derry C, Glasbey T (2012) The comparative performance of three brands of portable ATP-bioluminometer intended for use in hospital infection control. Healthcare Infect 17(3):91–97. doi:10.1071/HI12021

    Article  Google Scholar 

  • WHO (2009) Guidelines on hand hygiene in health care. First global patient safety challenge clean care is safer care. World Health Organization, Geneva. ISBN-13 978-92-4-159790-6

    Google Scholar 

  • Yeruham I, Elad D, Avidar Y, Goshen T (2006) A herd level analysis of urinary tract infection in dairy cattle. Vet J 171(1):172–176

    Article  CAS  PubMed  Google Scholar 

  • Yokoe DS, Mermel LA, Anderson DJ et al (2008) A compendium of strategies to prevent healthcare-associated infections in acute care hospitals. Infect Control Hosp Epidemiol 29(Suppl 1):S12–S21. doi:10.1086/591060

  • Zell C, Resch M, Rosenstein R et al (2008) Characterization of toxin production of coagulase-negative staphylococci isolated from foods and starter cultures. Int J Food Microbiol 127:246–251

    Article  CAS  PubMed  Google Scholar 

  • Zollfrank C, Gutbrod K, Wechsler P et al (2012) Antimicrobial activity of transition metal acid MoO3 prevents microbial growth on material surfaces. Mater Sci Eng, C 32(1):47–54. doi:10.1016/j.msec.2011.09.010

    Article  CAS  Google Scholar 

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Correspondence to Sabah A. A. Jassim .

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Jassim, S.A.A., Limoges, R.G. (2017). Control, Prevention and Rapid Detection of Methicillin-Resistant Staphylococcus aureus . In: Bacteriophages: Practical Applications for Nature's Biocontrol . Springer, Cham. https://doi.org/10.1007/978-3-319-54051-1_4

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