Isothiocyanates: An overview of their antimicrobial activity against human infections

Molecules

Volumn 23, Issue 3, 2018, Pages

  Romeo, Letizia ^a   Iori, Renato ^b   Rollin, Patrick ^c   Bramanti, Placido ^a   Mazzon, Emanuela ^a  

^a IRCCS CENTRO NEUROLESI BONINO PULEJO   (Italy)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^c UNIVERSITÉ D'ORLÉANS   (France)

Author keywords

Allyl isothiocyanate (AITC); Antibiotics; Benzyl isothiocyanate (BITC); Isothiocyanates (ITCs); Microbial infection; Moringin (MGN); Phenyl ethyl isothiocyanate (PEITC); Phenyl isothiocyanate (PITC); Sulforaphane (SFN)

Indexed keywords

ANTIINFECTIVE AGENT; BIOLOGICAL PRODUCT; ISOTHIOCYANIC ACID DERIVATIVE;

CHEMISTRY; HUMAN; INFECTION; METABOLISM;

ANTI-INFECTIVE AGENTS; BIOLOGICAL PRODUCTS; HUMANS; INFECTION; ISOTHIOCYANATES; METABOLIC NETWORKS AND PATHWAYS;

EID: 85043483935     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules23030624     Document Type: Review

References (104)

1. Petrovska, B.B. Historical review of medicinal plants' usage. Pharmacogn. Rev. 2012, 6, 1-5.
2. Cragg, G.M.; Pezzuto, J.M. Natural products as a vital source for the discovery of cancer chemotherapeutic and chemopreventive agents. Med. Princ. Pract. 2016, 25, 41-59.
3. Newman, D.J.; Cragg, G.M. Natural products as sources of new drugs from 1981 to 2014. J. Nat. Prod. 2016, 79, 629-661.
4. Thakur, S.; Sarkar, B.; Cholia, R.P.; Gautam, N.; Dhiman, M.; Mantha, A.K. Ape1/ref-1 as an emerging therapeutic target for various human diseases: Phytochemical modulation of its functions. Exp. Mol. Med. 2014, 46, e106.
5. Dillard, C.J.; German, J.B. Phytochemicals: Nutraceuticals and human health. J. Sci. Food Agric. 2000, 80, 1744-1756.
6. Hammer, K.A.; Carson, C.F.; Riley, T.V. Antimicrobial activity of essential oils and other plant extracts. J. Appl. Microbiol. 1999, 86, 985-990.
7. Arora, D.S.; Kaur, J. Antimicrobial activity of spices. Int. J. Antimicrob. Agents 1999, 12, 257-262.
8. Saladino, F.; Bordin, K.; Luciano, F.B.; Franzón, M.F.; Mañes, J.; Meca, G. Antimicrobial activity of the glucosinolates. In Glucosinolates, 1st ed.; Ramawat, K.G., Mérillon, J.-M., Eds.; Reference Series in Phytochemistry; Springer: Cham, Germany, 2017; pp. 249-274.
9. Tiwari, B.K.; Valdramidis, V.P.; O'Donnell, C.P.; Muthukumarappan, K.; Bourke, P.; Cullen, P.J. Application of natural antimicrobials for food preservation. J. Agric. Food Chem. 2009, 57, 5987-6000.
10. Romero, C.D.; Chopin, S.F.; Buck, G.; Martinez, E.; Garcia, M.; Bixby, L. Antibacterial properties of common herbal remedies of the southwest. J. Ethnopharmacol. 2005, 99, 253-257.
11. Guil-Guerrero, J.L.; Ramos, L.; Moreno, C.; Zuniga-Paredes, J.C.; Carlosama-Yepez, M.; Ruales, P. Antimicrobial activity of plant-food by-products: A review focusing on the tropics. Livest. Sci. 2016, 189, 32-49.
12. Dufour, V.; Stahl, M.; Baysse, C. The antibacterial properties of isothiocyanates. Microbiol. Soc. 2015, 161, 229-243.
13. Brabban, A.D.; Edwards, C. The effects of glucosinolates and their hydrolysis products on microbial growth. J. Appl. Bacteriol. 1995, 79, 171-177.
14. Blažević, I.; Montaut, S.; Burčul, F.; Rollin, P. Glucosinolates: Novel sources and biological potential. In Glucosinolates, 1st ed.; Ramawat, K.G., Mérillon, J.-M., Eds.; Reference Series in Phytochemistry; Springer: Cham, Germany, 2017; pp. 3-60.
15. Ishida, M.; Hara, M.; Fukino, N.; Kakizaki, T.; Morimitsu, Y. Glucosinolate metabolism, functionality and breeding for the improvement of brassicaceae vegetables. Breed. Sci. 2014, 64, 48-59.
16. Haristoy, X.; Angioi-Duprez, K.; Duprez, A.; Lozniewski, A. Efficacy of sulforaphane in eradicating Helicobacter pylori in human gastric xenografts implanted in nude mice. Antimicrob. Agents Chemother. 2003, 47, 3982-3984.
17. Yanaka, A.; Zhang, S.H.; Tauchi, M.; Suzuki, H.; Shibahara, T.; Matsui, H.; Nakahara, A.; Tanaka, N. Daily intake of sulforaphane-rich broccoli sprouts prevents progression of high salt diet-induced gastric atrophy in H. pylori-infected C57/BL6 mice in vivo. Gastroenterology 2003, 124, A5.
18. Jin, Y.; Wang, M.; Rosen, R.T.; Ho, C.T. Thermal degradation of sulforaphane in aqueous solution. J. Agric. Chem. 1999, 47, 3121-3123.
19. Fahey, J.W.; Zalcmann, A.T.; Talalay, P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 2001, 56, 5-51.
20. Agerbirk, N.; Olsen, C.E. Glucosinolate structures in evolution. Phytochemistry 2012, 77, 16-45.
21. Iori, R.; Rollin, P.; Streicher, H.; Thiem, J.; Palmieri, S. The myrosinase-glucosinolate interaction mechanism studied using some synthetic competitive inhibitors. FEBS Lett. 1996, 385, 87-90.
22. Bones, A.M.; Rossiter, J.T. The myrosinase-glucosinolate system, its organisation and biochemistry. Physiol. Plant. 1996, 97, 194-208.
23. Bones, A.M.; Rossiter, J.T. The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry 2006, 67, 1053-1067.
24. Traka, M.; Mithen, R. Glucosinolates, isothiocyanates and human health. Phytochem. Rev. 2009, 8, 269-282.
25. Sivapalan, T.; Melchini, A.; Saha, S.; Needs, P.W.; Traka, M.H.; Tapp, H.; Dainty, J.R.; Mithen, R.F. Bioavailability of glucoraphanin and sulforaphane from high-glucoraphanin broccoli. Mol. Nutr. Food Res. 2018.
26. Abd Rani, N.Z.; Husain, K.; Kumolosasi, E. Moringa genus: A review of phytochemistry and pharmacology. Front. Pharmacol. 2018.
27. Jung, I.L. Soluble extract from Moringa oleifera leaves with a new anticancer activity. PLoS ONE 2014, 9, e95492.
28. Giacoppo, S.; Rajan, T.S.; Iori, R.; Rollin, P.; Bramanti, P.; Mazzon, E. The alpha-cyclodextrin complex of the Moringa isothiocyanate suppresses lipopolysaccharide-induced inflammation in RAW 264.7 macrophage cells through Akt and p38 inhibition. Inflamm. Res. 2017, 66, 487-503.
29. Rajan, T.S.; Giacoppo, S.; Iori, R.; De Nicola, G.R.; Grassi, G.; Pollastro, F.; Bramanti, P.; Mazzon, E. Anti-inflammatory and antioxidant effects of a combination of cannabidiol and moringin in LPS-stimulated macrophages. Fitoterapia 2016, 112, 104-115.
30. Padla, E.P.; Solis, L.T.; Levida, R.M.; Shen, C.C.; Ragasa, C.Y. Antimicrobial Isothiocyanates from the Seeds of Moringa oleifera Lam. Z. Naturforsch. C 2012, 67, 557-564.
31. Dzotam, J.K.; Touani, F.K.; Kuete, V. Antibacterial and antibiotic-modifying activities of three food plants (Xanthosoma mafaffa Lam., Moringa oleifera (L.) Schott and Passiflora edulis Sims) against multidrug-resistant (MDR) Gram-negative bacteria. BMC Complement. Altern. Med. 2016, 16, 9.
32. Anwar, F.; Latif, S.; Ashraf, M.; Gilani, A.H. Moringa oleifera: A food plant with multiple medicinal uses. Phytother. Res. 2007, 21, 17-25.
33. Hashem, F.A.; Wahba, H.E. Isothiocyanates in myrosinase treated herb extract of Cleome chrysantha Decne. and their antimicrobial activities. Phytother. Res. 2000, 14, 284-287.
34. Muhaidat, R.; Al-Qudah, M.A.; Al-Shayeb, A.; Jacob, H.J.; Al-Jaber, H.I.; Hussein, E.; Al-Tarawneh, I.N.; Abu Orabi, S.T. Chemical profile and antibacterial activity of crude fractions and essential oils of Capparis ovata Desf. and Capparis spinosa L. (Capparaceae). Int. J. Integr. Biol. 2013, 14, 39-47.
35. Barba, F.J.; Nikmaram, N.; Roohinejad, S.; Khelfa, A.; Zhu, Z.; Koubaa, M. Bioavailability of glucosinolates and their breakdown products: Impact of processing. Front. Nutr. 2016, 3, 24.
36. Bollard, M.; Stribbling, S.; Mitchell, S.; Caldwell, J. The disposition of allyl isothiocyanate in the rat and mouse. Food Chem Toxicol. 1997, 35, 933-943.
37. Conaway, C.C.; Jiao, D.; Kohri, T.; Liebes, L.; Chung, F.L. Disposition and pharmacokinetics of phenethyl isothiocyanate and 6-phenylhexyl isothiocyanate in f344 rats. Drug Metab. Dispos. 1999, 27, 13-20.
38. Rouzaud, G.; Young, S.A.; Duncan, A.J. Hydrolysis of glucosinolates to isothiocyanates after ingestion of raw or microwaved cabbage by human volunteers. Cancer Epidemiol. Biomarker. Prev. 2004, 13, 125-131.
39. Getahun, S.M.; Chung, F.L. Conversion of glucosinolates to isothiocyanates in humans after ingestion of cooked watercress. Cancer Epidemiol. Biomark. Prev. 1999, 8, 447-451.
40. Walker, J.C. Studies on disease resistance in the onion. Proc. Natl. Acad. Sci. USA 1925, 11, 183-189.
41. Delaquis, P.J.; Mazza, G. Antimicrobial properties of isothiocyanates in food preservation. Food Technol. 1995, 49, 73-84.
42. Larkin, R.P.; Griffin, T.S. Control of soilborne potato diseases using Brassica green manures. Crop Prot. 2007, 26, 1067-1077.
43. Fahey, J.W.; Haristoy, X.; Dolan, P.M.; Kensler, T.W.; Scholtus, I.; Stephenson, K.K.; Talalay, P.; Lozniewski, A. Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo[a]pyrene-induced stomach tumors. Proc. Natl. Acad. Sci. USA 2002, 99, 7610-7615.
44. Ganin, H.; Rayo, J.; Amara, N.; Levy, N.; Krief, P.M.; Meijler, M. Sulforaphane and erucin, naturalisothiocyanates from broccoli, inhibit bacterial quorum sensing. Med. Chem. Comm. 2013, 4, 175-179.
45. Nowicki, D.; Rodzik, O.; Herman-Antosiewicz, A.; Szalewska-Palasz, A. Isothiocyanates as effective agents against enterohemorrhagic Escherichia coli: Insight to the mode of action. Sci. Rep. 2016, 6.
46. Dias, C.; Aires, A.; Bennett, R.N.; Rosa, E.A.S.; Saavedra, M.J. First study on antimicriobial activity and synergy between isothiocyanates and antibiotics against selected gram-negative and gram-positive pathogenic bacteria from clinical and animal source. Med. Chem. 2012, 8, 474-480.
47. Kim, M.G.; Lee, H.S. Growth-inhibiting activities of phenethyl isothiocyanate and its derivatives against intestinal bacteria. J. Food Sci. 2009, 74, M467-M471.
48. Kaiser, S.J.; Mutters, N.T.; Blessing, B.; Günther, F. Natural isothiocyanates express antimicrobial activity against developing and mature biofilms of Pseudomonas aeruginosa. Fitoterapia 2017, 119, 57-63.
49. Borges, A.; Abreu, A.C.; Ferreira, C.; Saavedra, M.J.; Simoes, L.C.; Simoes, M. Antibacterial activity and mode of action of selected glucosinolate hydrolysis products against bacterial pathogens. J. Food Sci. Technol. 2015, 52, 4737-4748.
50. Aires, A.; Mota, V.R.; Saavedra, M.J.; Rosa, E.A.S.; Bennett, R.N. The antimicrobial effects of glucosinolates and their respective enzymatic hydrolysis products on bacteria isolated from the human intestinal tract. J. Appl. Microbiol. 2009, 106, 2086-2095.
51. Dias, C.; Aires, A.; Saavedra, M.J. Antimicrobial activity of isothiocyanates from cruciferous plants against methicillin-resistant Staphylococcus aureus (MRSA). Int. J. Mol. Sci. 2014, 15, 19552-19561.
52. Sofrata, A.; Santangelo, E.M.; Azeem, M.; Borg-Karlson, A.K.; Gustafsson, A.; Pütsep, K. Benzyl isothiocyanate, a major component from the roots of Salvadora persica is highly active against Gram-negative bacteria. PLoS ONE 2011, 6, e23045.
53. Dufour, V.; Alazzam, B.; Ermel, G.; Thepaut, M.; Rossero, A.; Tresse, O.; Baysse, C. Antimicrobial activities of isothiocyanates against Campylobacter jejuni isolates. Front. Cell. Infect. Microbiol. 2012, 2, 53.
54. Dufour, V.; Stahl, M.; Rosenfeld, E.; Stintzi, A.; Baysse, C. Insights into the mode of action of benzyl isothiocyanate on Campylobacter jejuni. Appl. Environ. Microbiol. 2013, 79, 6958-6968.
55. Lu, Z.J.; Dockery, C.R.; Crosby, M.; Chavarria, K.; Patterson, B.; Giedd, M. Antibacterial activities of wasabi against Escherichia coli O157:H7 and Staphylococcus aureus. Front. Microbiol. 2016, 7, 1043.
56. Lin, C.M.; Preston, J.F., III; Wei, C.I. Antibacterial mechanism of allyl isothiocyanate. J. Food Prot. 2000, 63, 727-734.
57. Luciano, F.B.; Holley, R.A. Enzymatic inhibition by allyl isothiocyanate and factors affecting its antimicrobial action against Escherichia coliO157:H7. Int. J. Food Microbiol. 2009, 131, 240-245.
58. Jakobsen, T.H.; Bragason, S.K.; Phipps, R.K.; Christensen, L.D.; van Gennip, M.; Alhede, M.; Skindersoe, M.; Larsen, T.O.; Hoiby, N.; Bjarnsholt, T.; et al. Food as a source for quorum sensing inhibitors: Iberin from horseradish revealed as a quorum sensing inhibitor of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 2012, 78, 2410-2421.
59. Saleh, N.M.; Mabrouk, M.I.; Salem-Bekhit, M.M.; Hafez, E.H. Challenge of Moringa peregrine Forssk as an antimicrobial agent against multi-drug-resistant Salmonella sp. Biotechnol. Biotechnol. Eq. 2017, 31, 380-386.
60. Pal, S.K.; Mukherjee, P.K.; Saha, K.; Pal, M.; Saha, B.P. Antimicrobial action of the leaf extract of Moringa oleifera Lam. Anc. Sci. Life 1995, 14, 197-199.
61. Rahman, M.M.; Rahman, M.M.; Akhter, S.; Jamal, M.A.; Pandeya, D.R.; Haque, M.A.; Alam, M.F.; Rahman, A. Control of coliform bacteria detected from diarrhea associated patients by extracts of Moringa oleifera. Nepal Med. Coll. J. 2010, 12, 12-19.
62. Rahman, M.M.; Islam Sheik, M.M.; Sharmin, S.A.; Islam, M.S.; Rahman, M.A.; Rahman, M.M.; Alam, M.F. Antibacterial activity of leaves juice and extracts of Moringa oleifera Lam. (2n = 28) against some human pathogenic bacteria. Chiang-Mai Univ. J. Nat. Sci. 2009, 8, 219-227.
63. Peixoto, J.R.O.; Silva, G.C.; Costa, R.A.; Fontenelle, J.L.D.; Vieira, G.H.F.; Filho, A.A.F.; Vieira, R.H.S.D.F. In vitro antibacterial effect of aqueous and ethanolic Moringa leaf extracts. Asian Pac. J. Trop. Med. 2011, 4, 201-204.
64. Zaffer, M.; Ahmad, S.; Sharma, R.; Mahajan, S.; Gupta, A.; Agnihotri, R.K. Antibacterial activity of bark extracts of Moringa oleiferaLam. against some selected bacteria. Pak. J. Pharm. Sci. 2014, 27, 1857-1862.
65. Dalukdeniya, D.A.C.K.; De Silva, K.L.S.R.; Rathnayaka, R.M.U.S.K. Antimicrobial activity of different extracts of leaves bark and roots of Moringa oleifera (Lam). Int. J. Curr. Microbiol. Appl. Sci. 2016, 5, 687-691.
66. Vieira, G.H.F.; Mourao, J.A.; Angelo, A.M.; Costa, R.A.; Vieira, R.H.S.D. Antibacterial effect (in vitro) of Moringa oleifera and Annona muricata against Gram positive and Gram negative bacteria. Rev. Inst. Med. Trop. Sao Paulo 2010, 52, 129-132.
67. Walter, A.; Samuel, W.; Peter, A.; Joseph, O. Antibacterial activity of moringa oleifera and moringa stenopetala methanol and n-hexane seed extracts on bacteria implicated in water borne diseases. Afr J Microbiol. Res. 2011, 5, 153-157.
68. Galuppo, M.; Nicola, G.R.; Iori, R.; Dell'Utri, P.; Bramanti, P.; Mazzon, E. Antibacterial activity of glucomoringin bioactivated with myrosinase against two important pathogens affecting the health of long-term patients in hospitals. Molecules 2013, 18, 14340-14348.
69. Björkholm, N.; Zhukhovitsky, V.; Löfman, C.; Hultén, K.; Enroth, H.; Block, M.; Rigo, R.; Falk, P.; Engstrand, L. Helicobacter pylori entry into human gastric epithelial cells: A potential determinant of virulence, persistence, and treatment failures. Helicobacter 2000, 5, 148-154.
70. Brenciaglia, M.I.; Fornara, A.M.; Scaltrito, M.M.; Dubini, F. Helicobacter pylori: Cultivability and antibiotic susceptibility of coccoid forms. Int. J. Antimicrob. Agents 2000, 13, 237-241.
71. Engstrand, L.; Graham, D.; Scheynius, A.; Genta, R.M.; El-Zaatari, F. Is the sanctuary where Helicobacter pylori avoids antibacterial treatment intracellular? Am. J. Clin. Pathol. 1997, 108, 504-509.
72. Ohba, R.; Iijima, K. Pathogenesis and risk factors for gastric cancer after Helicobacter pylori eradication. World J. Gastrointest. Oncol. 2016, 8, 663-672.
73. Fahey, J.W.; Stephenson, K.K.; Wade, K.L.; Talalay, P. Urease from Helicobacter pylori is inactivated by sulforaphane and other isothiocyanates. Biochem. Biophys. Res. Commun. 2013, 435, 1-7.
74. Ha, N.C.; Oh, S.T.; Sung, J.Y.; Cha, K.A.; Lee, M.H.; Oh, B.H. Supramolecular assembly and acid resistance of Helicobacter pylori urease. Nat. Struct. Biol. 2001, 8, 505-509.
75. Hu, L.T.; Mobley, H.L. Purification and N-terminal analysis of urease from Helicobacter pylori. Infect. Immun. 1990, 58, 992-998.
76. Rood, J.I.; McClane, B.A.; Songer, J.G.; Titball, R.W. The Clostridia: Molecular Biology and Pathogenesis; Academic Press: London, UK, 1997.
77. Rupnik, M.; Wilcox, M.H.; Gerding, D.N. Clostridium difficile infection: New developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 2009, 7, 526-536.
78. Borriello, S.P.; Welch, A.R.; Larson, H.E.; Barclay, F.; Stringer, M.F.; Bartholomew, B.A. Enterotoxigenic Clostridium perfringens: A possible cause of antibiotic-associated diarrhoea. Lancet 1984, 1, 305-307.
79. Savidge, T.C.; Pan, W.H.; Newman, P.; O'Brien, M.; Anton, P.M.; Pothoulakis, C. Clostridium difficile toxin B is an inflammatory enterotoxin in human intestine. Gastroenterology 2003, 125, 413-420.
80. Niilo, L. Clostridium perfringens in animal disease: a review of current knowledge. Can. Vet. J. 1980, 21, 141-148.
81. Park, H.W.; Choi, K.D.; Shin, I.S. Antimicrobial activity of isothiocyanates (ITCs) extracted from horseradish (Armoracia rusticana) root against oral microorganisms. Biocontrol. Sci. 2013, 18, 163-168.
82. Rzewuska, K.; Korsak, D.; Maćkiw, E. Antibiotic resistance of bacteria Campylobacter sp. Przeglad Epidemiol. 2010, 64, 63-68.
83. Engberg, J.; Aarestrup, F.M.; Taylor, D.E.; Gerner-Smidt, P.; Nachamkin, I. Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: Resistance mechanisms and trends in human isolates. Emerg. Infect. Dis. 2001, 7, 24-34.
84. Dingle, K.E.; Colles, F.M.; Ure, R.; Wagenaar, J.A.; Duim, B.; Bolton, F.J.; Fox, A.J.; Wareing, D.R.A.; Maiden, M.C.J. Molecular characterization of Campylobacter jejuni clones: A basis for epidemiologic investigation. Emerg. Infect. Dis. 2002, 8, 949-955.
85. Feasey, N.A.; Dougan, G.; Kingsley, R.A.; Heyderman, R.S.; Gordon, M.A. Invasive non-typhoidal Salmonella disease: An emerging and neglected tropical disease in Africa. Lancet 2012, 379, 2489-2499.
86. Escobar-Paramo, P.; Clermont, O.; Blanc-Potard, A.B.; Bui, H.; Le Bouguenec, C.; Denamur, E. A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli. Mol. Biol. Evol. 2004, 21, 1085-1094.
87. Nataro, J.P.; Kaper, J.B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 1998, 11, 142-201.
88. Pacheco, A.R.; Sperandio, V. Shiga toxin in enterohemorrhagic E.coli: Regulation and novel anti-virulence strategies. Front. Cell. Infect. Microbiol. 2012, 2, 81.
89. Lebeaux, D.; Ghigo, J.M.; Beloin, C. Biofilm-related infections: Bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics. Microbiol. Mol. Biol. Rev. 2014, 78, 510-543.
90. Donlan, R.M. Biofilm formation: a clinically relevant microbiological process. Clin. Infect. Dis. 2001, 33, 1387-1392.
91. Bridier, A.; Sanchez-Vizuete, P.; Guilbaud, M.; Piard, J.-C.; Naitali, M.; Briandet, R. Biofilm-associated persistence of food-borne pathogens. Food Microbiol. 2015, 45, 167-178.
92. Velez Perez, A.L.; Schmidt-Malan, S.M.; Kohner, P.C.; Karau, M.J.; Greenwood-Quaintance, K.E.; Patel, R. In vitro activity of ceftolozane/tazobactam against clinical isolates of Pseudomonas aeruginosa in the planktonic and biofilm states. Diagn. Microbiol. Infect. Dis. 2016, 85, 356-359.
93. Defez, C.; Fabbro-Peray, P.; Bouziges, N.; Gouby, A.; Mahamat, A.; Daurès, J.P.; Sotto, A. Risk factors for multidrug-resistant Pseudomonas aeruginosa nosocomial infection. J. Hosp. Infect. 2004, 57, 209-216.
94. Van Delden, C.; Iglewski, B.H. Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg. Infect. Dis. 1998, 4, 551-560.
95. Li, Y.H.; Tian, X.L. Quorum sensing and bacterial social interactions in biofilms. Sensors 2012, 12, 2519-2538.
96. Hall, S.; McDermott, C.; Anoopkumar-Dukie, S.; McFarland, A.J.; Forbes, A.; Perkins, A.V.; Davey, A.K.; Chess-Williams, R.; Kiefel, M.J.; Arora, D.; et al. Cellular effects of pyocyanin, a secreted virulence factor of Pseudomonas aeruginosa. Toxins 2016, 9, 8.
97. Zulianello, L.; Canard, C.; Kohler, T.; Caille, D.; Lacroix, J.S.; Meda, P. Rhamnolipids are virulence factors that promote early infiltration of primary human airway epithelia by Pseudomonas aeruginosa. Infect. Immun. 2006, 74, 3134-3147.
98. Mittal, R.; Aggarwal, S.; Sharma, S.; Chhibber, S.; Harjai, K. Urinary tract infections caused by Pseudomonas aeruginosa: A minireview. J. Infect. Public Health 2009, 2, 101-111.
99. Jeong, S.J.; Yoon, S.S.; Bae, I.K.; Jeong, S.H.; Kim, J.M.; Lee, K. Risk factors for mortality in patients with bloodstream infections caused by carbapenem-resistant Pseudomonas aeruginosa: Clinical impact of bacterial virulence and strains on outcome. Diagn. Microbiol. Infect. Dis. 2014, 80, 130-135.
100. Kim, H.K.; Thammavongsa, V.; Schneewind, O.; Missiakas, D. Recurrent infections and immune evasion strategies of Staphylococcus aureus. Curr. Opin. Microbiol. 2012, 15, 92-99.
101. Montgomery, C.P.; Daniels, M.; Zhao, F.; Alegre, M.-L.; Chong, A.S.; Daum, R.S. Protective immunity against recurrent Staphylococcus aureus skin infection requires antibody and interleukin-17A. Infect. Immun. 2014, 82, 2125-2134.
102. Libert, M.; Elkholti, M.; Massaut, J.; Karmali, R.; Mascart, G.; Cherifi, S. Risk factors for meticillin resistance and outcome of Staphylococcus aureus bloodstream infection in a Belgian university hospital. J. Hosp. Infect. 2008, 68, 17-24.
103. Klein, E.; Smith, D.L.; Laxminarayan, R. Hospitalizations and deaths caused by methicillin-resistant Staphylococcus aureus, United States, 1999-2005. Emerg. Infect. Dis. 2007, 13, 1840-1846.
104. Elixhauser, A.; Steiner, C. Infections with methicillin-resistant Staphylococcus aureus (MRSA) in U.S. Hospitals, 1993-2005: Statistical brief #35. In Healthcare Cost and Utilization Project (HCUP) Statistical Briefs; Agency for Healthcare Research and Quality (US): Rockville, MD, USA, 2006.