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Erschienen in: Clinical Orthopaedics and Related Research® 2/2009

01.02.2009 | Original Article

The Influence of Maggot Excretions on PAO1 Biofilm Formation on Different Biomaterials

verfasst von: Gwendolyn Cazander, MD, Kiril E. B. van Veen, Lee H. Bouwman, MD, PhD, Alexandra T. Bernards, MD, PhD, Gerrolt N. Jukema, MD, PhD

Erschienen in: Clinical Orthopaedics and Related Research® | Ausgabe 2/2009

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Abstract

Biofilm formation in wounds and on biomaterials is increasingly recognized as a problem. It therefore is important to focus on new strategies for eradicating severe biofilm-associated infections. The beneficial effects of maggots (Lucilia sericata) in wounds have been known for centuries. We hypothesized sterile maggot excretions and secretions (ES) could prevent, inhibit, and break down biofilms of Pseudomonas aeruginosa (PAO1) on different biomaterials. Therefore, we investigated biofilm formation on polyethylene, titanium, and stainless steel. Furthermore, we compared the biofilm reduction capacity of Instar-1 and Instar-3 maggot ES and tested the temperature tolerance of ES. After biofilms formed in M63 nutrient medium on comb-forming models of the biomaterials, ES solutions in phosphate-buffered saline or M63 were added in different concentrations. PAO1 biofilms adhered tightly to polyethylene and titanium but weakly to stainless steel. Maggot ES prevent and inhibit PAO1 biofilm formation and even break down existing biofilms. ES still had considerable biofilm reduction properties after storage at room temperature for 1 month. ES from Instar-3 maggots were more effective than ES from Instar-1 maggots. These results may be relevant to patient care as biofilms complicate the treatment of infections associated with orthopaedic implants.
Literatur
1.
Zurück zum Zitat Baer WS. The treatment of chronic osteomyelitis with the maggot (larvae of the blowfly). J Bone Joint Surg. 1931;13:438–475. Baer WS. The treatment of chronic osteomyelitis with the maggot (larvae of the blowfly). J Bone Joint Surg. 1931;13:438–475.
2.
Zurück zum Zitat Bexfield A, Nigam Y, Thomas S, Ratcliffe NA. Detection and partial characterisation of two antibacterial factors from the excretions/secretions of the medicinal maggot Lucilia sericata and their activity against methicillin-resistant Staphylococcus aureus (MRSA). Microbes Infect. 2004;14:1297–1304. CrossRef Bexfield A, Nigam Y, Thomas S, Ratcliffe NA. Detection and partial characterisation of two antibacterial factors from the excretions/secretions of the medicinal maggot Lucilia sericata and their activity against methicillin-resistant Staphylococcus aureus (MRSA). Microbes Infect. 2004;14:1297–1304. CrossRef
3.
Zurück zum Zitat Casu RE, Pearson RD, Jarmey JM, Cadogan LC, Riding GA, Tellam RL. Extretory/secretory chymotrypsin from Lucilia cuprina: purification enzymatic specificity and amino acid sequence deduced from mRNA. Insect Mol Biol. 1994;3:201–211.PubMedCrossRef Casu RE, Pearson RD, Jarmey JM, Cadogan LC, Riding GA, Tellam RL. Extretory/secretory chymotrypsin from Lucilia cuprina: purification enzymatic specificity and amino acid sequence deduced from mRNA. Insect Mol Biol. 1994;3:201–211.PubMedCrossRef
4.
Zurück zum Zitat Chambers L, Woodrow S, Brown AP, Harris PD, Philips D, Hall M, Church JC, Pritchard DI. Degradation of extracellular matrix components by defined proteinases from the greenbottle larva Lucilia sericata used for the clinical debridement of non-healing wounds. Br J Dermatol. 2003;148:14–23.PubMedCrossRef Chambers L, Woodrow S, Brown AP, Harris PD, Philips D, Hall M, Church JC, Pritchard DI. Degradation of extracellular matrix components by defined proteinases from the greenbottle larva Lucilia sericata used for the clinical debridement of non-healing wounds. Br J Dermatol. 2003;148:14–23.PubMedCrossRef
6.
Zurück zum Zitat Costerton JW. Biofilm theory can guide the treatment of device-related orthopaedic infections. Clin Orthop Relat Res. 2005;437:7–11.PubMedCrossRef Costerton JW. Biofilm theory can guide the treatment of device-related orthopaedic infections. Clin Orthop Relat Res. 2005;437:7–11.PubMedCrossRef
7.
Zurück zum Zitat Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284:1318–1322.PubMedCrossRef Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284:1318–1322.PubMedCrossRef
8.
Zurück zum Zitat Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilm: from the natural environment to infectious diseases. Nat Rev Microbiol. 2004;2:95–108.PubMedCrossRef Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilm: from the natural environment to infectious diseases. Nat Rev Microbiol. 2004;2:95–108.PubMedCrossRef
9.
Zurück zum Zitat Harris LG, Meredith DO, Eschbach L, Richards RG. Staphylococcus aureus adhesion to standard micro-rough and electropolished implant materials. J Mater Sci Mater Med. 2007;18:1151–1156.PubMedCrossRef Harris LG, Meredith DO, Eschbach L, Richards RG. Staphylococcus aureus adhesion to standard micro-rough and electropolished implant materials. J Mater Sci Mater Med. 2007;18:1151–1156.PubMedCrossRef
10.
Zurück zum Zitat Horobin AJ, Shakesheff KM, Pritchard DI. Promotion of human dermal fibroblast migration, matrix remodelling and modification of fibroblast morphology within a novel 3D model by Lucilia sericata larval secretions. J Invest Dermatol. 2006;126:1410–1418.PubMedCrossRef Horobin AJ, Shakesheff KM, Pritchard DI. Promotion of human dermal fibroblast migration, matrix remodelling and modification of fibroblast morphology within a novel 3D model by Lucilia sericata larval secretions. J Invest Dermatol. 2006;126:1410–1418.PubMedCrossRef
11.
Zurück zum Zitat Jukema GN, Menon AG, Bernards AT, Steenvoorde P, Taheri Rastegar A, Van Dissel JT. Amputation-sparing treatment by nature: ‘surgical’ maggots revisited. Clin Infect Dis. 2002;35:1566–1571.PubMedCrossRef Jukema GN, Menon AG, Bernards AT, Steenvoorde P, Taheri Rastegar A, Van Dissel JT. Amputation-sparing treatment by nature: ‘surgical’ maggots revisited. Clin Infect Dis. 2002;35:1566–1571.PubMedCrossRef
12.
Zurück zum Zitat Kadurugamuwa JL, Francis KP. Bioluminescent imaging of bacterial biofilm infections in vivo. Methods Mol Biol. 2008;431:225–239.PubMedCrossRef Kadurugamuwa JL, Francis KP. Bioluminescent imaging of bacterial biofilm infections in vivo. Methods Mol Biol. 2008;431:225–239.PubMedCrossRef
13.
Zurück zum Zitat Kerridge A, Lappin-Scott H, Stevens JR. Antibacterial properties of larval secretions of the blowfly, Lucilia sericata. Med Vet Entomol. 2005;3:333–337.CrossRef Kerridge A, Lappin-Scott H, Stevens JR. Antibacterial properties of larval secretions of the blowfly, Lucilia sericata. Med Vet Entomol. 2005;3:333–337.CrossRef
14.
Zurück zum Zitat King EO, Ward MK, Raney DE. Two simple media for the demonstration of pyocyanin and fluorescein. J Lab Clin Med. 1954;44:301–307.PubMed King EO, Ward MK, Raney DE. Two simple media for the demonstration of pyocyanin and fluorescein. J Lab Clin Med. 1954;44:301–307.PubMed
15.
16.
Zurück zum Zitat Meisenberg G, Simmons WH. Principles of Medical Biochemistry. St Louis, MO: Mosby; 1998. Meisenberg G, Simmons WH. Principles of Medical Biochemistry. St Louis, MO: Mosby; 1998.
17.
Zurück zum Zitat Mumcuoglu K, Miller J, Mumcuoglu M, Friger F, Tarshis M. Destruction of bacteria in the digestive tract of the maggot of Lucilia sericata (Diptera: Calliphoridae). J Med Entomol. 2001;38:161–166.PubMed Mumcuoglu K, Miller J, Mumcuoglu M, Friger F, Tarshis M. Destruction of bacteria in the digestive tract of the maggot of Lucilia sericata (Diptera: Calliphoridae). J Med Entomol. 2001;38:161–166.PubMed
18.
Zurück zum Zitat Nablo BJ, Prichard HL, Butler RD, Klitzman B, Schoenfisch MH. Inhibition of implant-associated infections via nitric oxide release. Biomaterials. 2005;26:6984–6990.PubMedCrossRef Nablo BJ, Prichard HL, Butler RD, Klitzman B, Schoenfisch MH. Inhibition of implant-associated infections via nitric oxide release. Biomaterials. 2005;26:6984–6990.PubMedCrossRef
19.
Zurück zum Zitat Neut D, Hendriks JG, van Horn JR, van der Mei HC, Busscher HJ. Pseudomonas aeruginosa biofilm formation and slime excretion on antibiotic loaded bone cement. Acta Orthop. 2005;76:109–114.PubMedCrossRef Neut D, Hendriks JG, van Horn JR, van der Mei HC, Busscher HJ. Pseudomonas aeruginosa biofilm formation and slime excretion on antibiotic loaded bone cement. Acta Orthop. 2005;76:109–114.PubMedCrossRef
21.
Zurück zum Zitat O’Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol. 1998;28:449–461.PubMedCrossRef O’Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol. 1998;28:449–461.PubMedCrossRef
22.
Zurück zum Zitat van der Plas MJ, Jukema GN, Wai SW, Dogterom-Ballering HC, Lagendijk EL, van Gulpen C, van Dissel JT, Bloemberg GV, Nibbering PH. Maggot excretions/secretions are differentially effective against biofilm of Staphylococcus aureus and Pseudomonas aeruginosa. J Antimicrob Chemother. 2008;61:117–122.PubMedCrossRef van der Plas MJ, Jukema GN, Wai SW, Dogterom-Ballering HC, Lagendijk EL, van Gulpen C, van Dissel JT, Bloemberg GV, Nibbering PH. Maggot excretions/secretions are differentially effective against biofilm of Staphylococcus aureus and Pseudomonas aeruginosa. J Antimicrob Chemother. 2008;61:117–122.PubMedCrossRef
23.
Zurück zum Zitat Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol. 2002;184:1140–1154.PubMedCrossRef Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol. 2002;184:1140–1154.PubMedCrossRef
24.
Zurück zum Zitat Sherman RA, Hall MJR, Thomas S. Medicinal maggots: an ancient remedy for some contemporary afflictions. Annu Rev Entomol. 2000;45:55–81.PubMedCrossRef Sherman RA, Hall MJR, Thomas S. Medicinal maggots: an ancient remedy for some contemporary afflictions. Annu Rev Entomol. 2000;45:55–81.PubMedCrossRef
25.
Zurück zum Zitat Sherman RA, Pechter EA. Maggot therapy: a review of the therapeutic applications of fly larvae in human medicine, especially for treating osteomyelitis. Med Vet Entomol. 1988;2:225–230.PubMedCrossRef Sherman RA, Pechter EA. Maggot therapy: a review of the therapeutic applications of fly larvae in human medicine, especially for treating osteomyelitis. Med Vet Entomol. 1988;2:225–230.PubMedCrossRef
26.
Zurück zum Zitat Sritharan M, Shritharan V. Emerging problems in the management of infectious diseases: the biofilms. Indian J Med Microbiol. 2004;22:140–142.PubMed Sritharan M, Shritharan V. Emerging problems in the management of infectious diseases: the biofilms. Indian J Med Microbiol. 2004;22:140–142.PubMed
27.
Zurück zum Zitat Steenvoorde P, Jukema GN. The antimicrobial activity of maggots: in-vivo results. J Tissue Viability. 2004;14:97–101.PubMed Steenvoorde P, Jukema GN. The antimicrobial activity of maggots: in-vivo results. J Tissue Viability. 2004;14:97–101.PubMed
28.
Zurück zum Zitat Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358:135–138.PubMedCrossRef Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358:135–138.PubMedCrossRef
29.
Zurück zum Zitat Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock RE, Lory S, Olson MV. Complete genome sequence of Pseudomonas PAO1, an opportunistic pathogen. Nature. 2000;406:947–948.CrossRef Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock RE, Lory S, Olson MV. Complete genome sequence of Pseudomonas PAO1, an opportunistic pathogen. Nature. 2000;406:947–948.CrossRef
30.
Zurück zum Zitat Tanyuksel M, Araz E, Dundar K, Uzun G, Gumus T, Alten B, Saylam F, Taylan-Ozkan A, Mumcuoglu KY. Maggot debridement therapy in the treatment of chronic wounds in a military hospital setup in Turkey. Dermatology. 2005;210:115–118.PubMedCrossRef Tanyuksel M, Araz E, Dundar K, Uzun G, Gumus T, Alten B, Saylam F, Taylan-Ozkan A, Mumcuoglu KY. Maggot debridement therapy in the treatment of chronic wounds in a military hospital setup in Turkey. Dermatology. 2005;210:115–118.PubMedCrossRef
31.
Zurück zum Zitat Thomas S, Jones M, Shutler S, Andrews A. Wound care: all you need to know about maggots. Nurs Times. 1996;92:63–70.PubMed Thomas S, Jones M, Shutler S, Andrews A. Wound care: all you need to know about maggots. Nurs Times. 1996;92:63–70.PubMed
32.
Zurück zum Zitat Trampuz A, Widmer AF. Infections associated with orthopedic implants. Curr Opin Infect Dis. 2006;19:349–356.PubMedCrossRef Trampuz A, Widmer AF. Infections associated with orthopedic implants. Curr Opin Infect Dis. 2006;19:349–356.PubMedCrossRef
33.
Zurück zum Zitat Vistnes L, Lee R, Ksander A. Proteolytic activity of blowfly larvae secretions in experimental burns. Surgery. 1981;90:835–841.PubMed Vistnes L, Lee R, Ksander A. Proteolytic activity of blowfly larvae secretions in experimental burns. Surgery. 1981;90:835–841.PubMed
34.
Zurück zum Zitat Wainwright M. Miracle Cure: The Story of Penicillin and the Golden Age of Antibiotics. Oxford, UK: Basil Blackwell; 1990. Wainwright M. Miracle Cure: The Story of Penicillin and the Golden Age of Antibiotics. Oxford, UK: Basil Blackwell; 1990.
35.
Zurück zum Zitat Wang J, Wang S, Zhao G, Wang Z, Lineaweaver WC, Zhang F. Treatment of infected wounds with maggot therapy after replantation. J Reconstr Microsurg. 2006;22:277–280.PubMedCrossRef Wang J, Wang S, Zhao G, Wang Z, Lineaweaver WC, Zhang F. Treatment of infected wounds with maggot therapy after replantation. J Reconstr Microsurg. 2006;22:277–280.PubMedCrossRef
36.
Zurück zum Zitat Woodworth BA, Tamashiro E, Bhargave G, Cohen NA, Palmer JN. An in vitro model of Pseudomonas aeruginosa biofilms on viable airway epithelial cell monolayers. Am J Rhinol. 2008;22:235–238.PubMedCrossRef Woodworth BA, Tamashiro E, Bhargave G, Cohen NA, Palmer JN. An in vitro model of Pseudomonas aeruginosa biofilms on viable airway epithelial cell monolayers. Am J Rhinol. 2008;22:235–238.PubMedCrossRef
Metadaten
Titel
The Influence of Maggot Excretions on PAO1 Biofilm Formation on Different Biomaterials
verfasst von
Gwendolyn Cazander, MD
Kiril E. B. van Veen
Lee H. Bouwman, MD, PhD
Alexandra T. Bernards, MD, PhD
Gerrolt N. Jukema, MD, PhD
Publikationsdatum
01.02.2009
Verlag
Springer-Verlag
Erschienen in
Clinical Orthopaedics and Related Research® / Ausgabe 2/2009
Print ISSN: 0009-921X
Elektronische ISSN: 1528-1132
DOI
https://doi.org/10.1007/s11999-008-0555-2

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