The role of bacterial biofilms in chronic infections

APMIS - Tập 121 Số s136 - Trang 1-58 - 2013
Thomas Bjarnsholt1
1Københavns Universitet København N Denmark

Tóm tắt

Acute infections caused by pathogenic bacteria have been studied extensively for well over 100 years. These infections killed millions of people in previous centuries, but they have been combated effectively by the development of modern vaccines, antibiotics and infection control measures. Most research into bacterial pathogenesis has focused on acute infections, but these diseases have now been supplemented by a new category of chronic infections caused by bacteria growing in slime‐enclosed aggregates known as biofilms. Biofilm infections, such as pneumonia in cystic fibrosis patients, chronic wounds, chronic otitis media and implant‐ and catheter‐associated infections, affect millions of people in the developed world each year and many deaths occur as a consequence. In general, bacteria have two life forms during growth and proliferation. In one form, the bacteria exist as single, independent cells (planktonic) whereas in the other form, bacteria are organized into sessile aggregates. The latter form is commonly referred to as the biofilm growth phenotype. Acute infections are assumed to involve planktonic bacteria, which are generally treatable with antibiotics, although successful treatment depends on accurate and fast diagnosis. However, in cases where the bacteria succeed in forming a biofilm within the human host, the infection often turns out to be untreatable and will develop into a chronic state. The important hallmarks of chronic biofilm‐based infections are extreme resistance to antibiotics and many other conventional antimicrobial agents, and an extreme capacity for evading the host defences. In this thesis, I will assemble the current knowledge on biofilms with an emphasis on chronic infections, guidelines for diagnosis and treatment of these infections, before relating this to my previous research into the area of biofilms. I will present evidence to support a view that the biofilm lifestyle dominates chronic bacterial infections, where bacterial aggregation is the default mode, and that subsequent biofilm development progresses by adaptation to nutritional and environmental conditions. I will make a series of correlations to highlight the most important aspects of biofilms from my perspective, and to determine what can be deduced from the past decades of biofilm research. I will try to bridgein vitroandin vivoresearch and propose methods for studying biofilms based on this knowledge. I will compare how bacterial biofilms exist in stable ecological habitats and opportunistically in unstable ecological habitats, such as infections. Bacteria have a similar lifestyle (the biofilm) in both habitats, but the fight for survival and supremacy is different. On the basis of this comparison, I will hypothesize how chronic biofilm infections are initiated and how bacteria live together in these infections. Finally, I will discuss different aspects of biofilm infection diagnosis. Hopefully, this survey of current knowledge and my proposed guidelines will provide the basis and inspiration for more research, improved diagnostics, and treatments for well‐known biofilm infections and any that may be identified in the future.

Từ khóa


Tài liệu tham khảo

10.1111/j.1574-695X.2010.00714.x

Atlas RM, 1997, Microbial Ecology

10.1146/annurev.mi.49.100195.003431

10.1289/ehp.98106a604

10.1098/rstl.1684.0030

Henrici AT, 1933, Studies of freshwater bacteria, J Bacteriol, 25, 2132, 10.1128/jb.25.3.277-287.1933

RogovskaT LazarevaMF.Microbiological characteristics of biofilm purifying hydrogen sulphide containing sewage.1961.

HøibyN.Pseudomonas aeruginosa infection in cystic fibrosis.University of Copenhagen 1977.

10.1038/scientificamerican0178-86

10.1139/m81-143

10.1146/annurev.mi.41.100187.002251

10.1128/jb.176.8.2137-2142.1994

10.1126/science.284.5418.1318

10.1007/978-3-540-68022-2_5

10.1038/nrmicro1743

10.1016/j.ijantimicag.2009.12.011

10.1128/AAC.33.10.1824

10.3201/eid0809.020063

Zimmerli W, 2010, Biofilm Infections, 91

10.1016/S0140-6736(11)60988-4

10.1177/1753465810368552

10.1046/j.1365-2958.2003.03677.x

10.1046/j.1365-2958.2003.03525.x

10.1128/jb.184.4.1140-1154.2002

10.1371/journal.pone.0027943

10.1016/S0076-6879(99)10004-1

10.1128/AEM.68.5.2495-2502.2002

10.1111/j.1462-2920.2005.00775.x

10.1038/35023079

10.1007/s00216-006-0774-x

10.1111/j.1365-2672.2007.03413.x

10.1172/JCI0213870

10.1136/thx.2009.114512

10.1128/AAC.47.1.317-323.2003

Semmler AB, 1999, A re‐examination of twitching motility in Pseudomonas aeruginosa, Microbiology, 145, 2863, 10.1099/00221287-145-10-2863

10.1146/annurev.micro.54.1.49

10.1186/gb-2003-4-6-219

10.1128/AEM.68.9.4457-4464.2002

Reimmann C, 2002, Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1, Microbiology, 148, 923, 10.1099/00221287-148-4-923

10.1017/S1479050505001699

10.1186/1471-2180-10-294

10.1128/JCM.43.10.5247-5255.2005

10.1126/science.280.5361.295

Bjarnsholt T, 2005, Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum‐sensing dependent, Microbiology, 151, 373, 10.1099/mic.0.27463-0

10.1146/annurev.micro.56.012302.160705

10.1099/mic.0.27415-0

10.1099/mic.0.26829-0

10.1016/j.tim.2008.11.001

10.1371/journal.pone.0006289

10.1128/AEM.67.12.5608-5613.2001

Stapper AP, 2004, Alginate production affects Pseudomonas aeruginosa biofilm development and architecture, but is not essential for biofilm formation, J Med Microbiol, 53, 679, 10.1099/jmm.0.45539-0

10.1128/JB.185.15.4585-4592.2003

10.1111/j.1365-2958.2007.05772.x

10.1016/j.ahj.2003.09.018

10.1046/j.1469-0691.2002.00427.x

10.1111/j.1574-6968.2004.tb09643.x

10.1046/j.1365-2958.2001.02337.x

10.1099/00221287-11-1-123

10.1371/journal.ppat.1000354

10.1111/j.1365-2958.2005.05008.x

10.1126/science.295.5559.1487

10.1371/journal.pone.0005822

10.1073/pnas.0610226104

10.1111/j.1365-2958.2009.06991.x

10.1128/IAI.01117-06

10.1046/j.1365-2958.2003.03833.x

Matsuyama T, 1990, Surface‐active novel glycolipid and linked 3‐hydroxy fatty acids produced by Serratia rubidaea, J Bacteriol, 172, 3015, 10.1128/jb.172.6.3015-3022.1990

10.1128/JB.185.3.1027-1036.2003

10.1128/JB.01515-06

10.1186/1471-2180-5-30

10.1111/j.1574-695X.2010.00690.x

10.1016/j.mib.2008.09.015

10.1128/JB.00858-07

10.1128/JB.183.3.1047-1057.2001

10.1016/0891-5849(89)90078-6

10.1111/j.1365-2672.1992.tb05009.x

10.1016/0014-5793(72)80685-9

Pedersen SS, 1989, Purification, characterization, and immunological cross‐reactivity of alginates produced by mucoid Pseudomonas aeruginosa from patients with cystic fibrosis, J Clin Microbiol, 27, 691, 10.1128/jcm.27.4.691-699.1989

10.1016/S1569-1993(02)00104-2

Høiby N, 1974, Pseudomonas aeruginosa infection in cystic fibrosis. Relationship between mucoid strains of Pseudomonas aeruginosa and the humoral immune response, Acta Pathol Microbiol Scand [B] Microbiol Immunol, 82, 551

10.1073/pnas.1231792100

10.1086/431516

10.1111/j.1365-2958.2009.06795.x

10.1016/j.mib.2007.09.010

10.1111/j.1574-695X.2012.00956.x

10.1007/s00248-006-9063-7

10.1093/jac/dkp165

10.1371/journal.pone.0005724

10.1128/JB.00257-06

10.14219/jada.archive.2009.0049

10.1038/nature08790

10.1128/CMR.15.2.167-193.2002

10.1016/j.micinf.2003.08.009

10.1038/416740a

10.1128/AAC.48.4.1168-1174.2004

10.1128/AAC.31.2.230

10.1128/JB.183.18.5213-5222.2001

10.1111/j.1348-0421.2004.tb03533.x

10.1098/rstb.2009.0037

10.1111/j.1574-6976.2011.00295.x

Giedraitiene A, 2011, Antibiotic resistance mechanisms of clinically important bacteria, Medicina (Kaunas), 47, 137

10.1111/j.1699-0463.1994.tb05219.x

10.1016/j.ajic.2006.05.219

10.1371/journal.ppat.1000213

10.1038/nrmicro1838

10.1128/AEM.70.10.6188-6196.2004

10.1128/AEM.00710-08

Hoyle BD, 1991, Bacterial resistance to antibiotics: the role of biofilms, Prog Drug Res, 37, 91

10.1007/s11908-008-0006-y

10.1093/jac/22.6.777

10.1093/jac/dkn462

10.1128/AAC.48.1.48-52.2004

10.1128/AAC.48.7.2659-2664.2004

10.1128/AEM.69.4.2313-2320.2003

10.1111/j.1365-2958.2008.06152.x

Haagensen JA, 2006, Differentiation and distribution of colistin/SDS tolerant cells in Pseudomonas aeruginosa flow‐cell biofilms, J Bacteriol, 189, 28, 10.1128/JB.00720-06

10.1128/CMR.16.2.273-307.2003

10.1016/S0065-2164(04)54007-8

10.1007/s004230050196

10.1128/IAI.70.11.6339-6345.2002

10.1371/journal.pone.0002744

10.1111/j.1462-2920.2004.00556.x

10.1073/pnas.0505350102

10.1164/ajrccm/140.6.1650

10.1099/mic.0.031443-0

10.1016/S0140-6736(01)05321-1

10.1016/S1286-4579(00)01349-6

10.1099/mic.0.27955-0

10.1038/nrmicro1180

10.1038/ismej.2008.47

10.1128/JB.01581-07

10.1128/jb.176.2.269-275.1994

Manefield M, 2002, Quorum sensing in context: out of molecular biology and into microbial ecology, Microbiology, 148, 3762, 10.1099/00221287-148-12-3762

10.1093/molbev/msh097

10.1038/208155a0

10.1128/jb.104.1.313-322.1970

10.1111/j.1365-2958.1995.mmi_17020333.x

10.1093/emboj/cdg366

10.1128/JB.185.7.2080-2095.2003

10.1128/JB.185.7.2066-2079.2003

10.1128/MMBR.56.4.662-676.1992

10.1128/JB.187.5.1799-1814.2005

10.1099/mic.0.27715-0

Wu H, 2001, Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection, Microbiology, 147, 1105, 10.1099/00221287-147-5-1105

10.1073/pnas.92.14.6424

10.1046/j.1365-2958.2001.02420.x

10.1093/jac/49.2.309

Hentzer M, 2002, Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound, Microbiology, 148, 87, 10.1099/00221287-148-1-87

10.1046/j.1365-2958.1999.01672.x

10.1093/jac/dks002

10.1146/annurev.genet.35.102401.090913

10.1073/pnas.1934514100

10.4161/cib.3.2.10429

10.1073/pnas.052694299

10.1046/j.1365-2672.2001.01339.x

10.1073/pnas.96.24.13904

10.1128/JB.181.6.1703-1712.1999

10.1111/j.1365-2958.1996.tb02495.x

10.1128/JB.182.21.5990-5996.2000

Huber B, 2001, The cep quorum‐sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility, Microbiology, 147, 2517, 10.1099/00221287-147-9-2517

10.1016/0092-8674(94)90313-1

10.1046/j.1365-2958.2003.03672.x

10.1016/j.ijmm.2006.01.038

10.1016/j.mib.2009.01.005

10.1172/JCI20195

10.1128/IAI.68.5.2579-2586.2000

10.1074/jbc.M109.031757

10.3109/10408417709102809

10.1038/scientificamerican0969-146

10.1139/m77-249

10.1007/s10126-007-9001-9

10.1016/j.ijheh.2010.05.003

10.1023/A:1020586312170

Kelstrup J, 1977, Microbial aggregate contamination of water lines in dental equipment and its control, Acta Pathol Microbiol Scand B, 85, 177

Larsen T, 2008, Vandkvaliteten i danske dentalunits med og uden kimanlæg, Tandlægebladet, 112, 1316

10.1016/j.femsec.2004.06.005

10.1128/AEM.65.11.5107-5116.1999

10.1128/AEM.65.7.3182-3191.1999

10.1128/AEM.62.5.1656-1663.1996

10.1128/AEM.59.11.3840-3849.1993

10.1111/j.1462-2920.2005.00973.x

10.1094/PHYTO.2002.92.12.1329

10.1094/PHYTO.2004.94.11.1259

10.1111/j.1574-6941.2008.00465.x

Theilade E, 1970, Denal Plaque, 27

10.1902/jop.1975.46.1.10

10.1128/JB.00983-08

10.1128/AEM.72.4.2837-2848.2006

10.1128/JB.185.11.3400-3409.2003

Nyvad B, 1993, Microbial colonization of human tooth surfaces, APMIS Suppl, 32, 1

10.1177/08959374940080022001

10.1159/000159604

10.1128/MMBR.62.1.71-109.1998

10.1099/mic.0.027706-0

10.1111/j.1600-0722.2007.00494.x

10.1111/j.1600-0757.2005.00107.x

10.1126/science.1110591

10.1002/ibd.20176

10.1097/00006454-200205000-00012

10.1128/AEM.68.9.4225-4232.2002

Domingue PA, 1991, The human vagina: normal flora considered as an in situ tissue‐associated, adherent biofilm, Genitourin Med, 67, 226

10.1007/978-3-540-68022-2_4

10.1111/j.1440-1746.1993.tb01171.x

10.1155/2008/613979

10.1111/j.1365-2133.1980.tb08139.x

10.1023/A:1021271028979

Høiby N, 2008, Klinisk mikrobiologi og infektionsmedicin

10.1038/nm0706-736

10.12968/jowc.2010.19.2.46966

Marsh PD, 2009, Dental plaque as a biofilm: the significance of pH in health and caries, Compend Contin Educ Dent, 30, 76

Hodson JJ, 1955, A histopathological study of the bacterial plaque in relation to the destruction of enamel, dentine and bone with special reference to dental caries, Proc R Soc Med, 48, 641

10.1016/0003-9969(68)90023-X

10.1111/j.1600-051X.1977.tb00047.x

10.1111/j.1600-0765.1986.tb01483.x

10.1371/journal.pone.0009321

10.1128/iai.28.2.546-556.1980

10.1111/j.1524-475X.2007.00321.x

10.1001/jama.296.2.202

10.1161/01.CIR.66.6.1339

10.1099/jmm.0.46022-0

10.1128/JCM.18.6.1388-1398.1983

10.1128/JCM.19.5.687-693.1984

10.1159/000319396

10.1097/IOP.0b013e3181cff61f

10.1126/science.4001933

10.1128/JCM.22.6.924-933.1985

10.1159/000079994

10.1097/01.mlg.0000161346.30752.18

10.1097/01.mlg.0000221954.05467.54

10.1007/s00405-011-1683-y

10.1161/01.CIR.61.2.374

10.1128/JCM.40.7.2689-2690.2002

10.1016/S0022-5347(17)37247-6

10.1002/pros.2990230204

10.1016/S0924-8579(99)00136-3

10.1136/bjo.79.9.864

10.1111/j.1365-2672.2007.03287.x

10.1128/JCM.42.8.3549-3557.2004

10.1111/j.1742-481X.2006.00159.x

10.1186/1471-2180-8-43

10.1111/j.1524-475X.2007.00303.x

10.1097/SPC.0b013e328331d40c

10.1001/archdermatol.2009.246

10.1371/journal.pone.0006462

10.1111/j.1524-475X.2009.00561.x

10.1111/j.1699-0463.1996.tb04955.x

10.1111/j.1440-0960.1992.tb00083.x

10.1371/journal.pone.0020492

10.1038/sj.ijir.3901093

Percival SL, 2004, Biofilms and their potential role in wound healing, Wounds, 16

10.1007/s11892-006-0076-x

Mertz PM, 2003, Cutaneous biofilms: friend or foe?, Wounds, 15, 129

10.1128/JCM.01395-09

10.1002/ppul.10135

10.1164/rccm.200304-505SO

10.1126/science.2570460

10.1126/science.2475911

10.1126/science.2772657

10.1016/S0169-409X(02)00144-8

10.1097/00063198-200311000-00007

10.1046/j.1365-2958.2003.03672.x

10.1111/j.1651-2227.1983.tb09789.x

10.1136/thorax.55.5.349

10.1186/1741-7015-9-32

10.1016/0140-6736(93)92422-P

10.1001/jama.2010.1651

10.1097/INF.0b013e3181b6d81a

Leach AJ, 2006, Antibiotics for the prevention of acute and chronic suppurative otitis media in children, Cochrane Database Syst Rev, CD004401

10.1086/597042

10.1128/IAI.72.1.106-113.2004

10.1128/IAI.73.6.3210-3218.2005

10.1097/00005537-200112000-00001

10.1001/jama.279.4.296

10.1016/j.otohns.2009.08.010

10.1097/INF.0b013e318154b273

10.1016/S0194-59980301395-0

10.1016/j.ijporl.2009.05.016

10.1128/JCM.00756-10

10.1097/01.prs.0000234900.26676.0b

10.1111/j.1524-4725.2007.33357.x

10.1007/s00266-004-0113-6

10.1007/s00238-005-0005-2

10.1111/j.1524-4725.2009.01338.x

10.1111/j.1574-695X.2007.00357.x

10.2500/ajra.2009.23.3319

10.1097/MOO.0b013e3282fdc6d5

10.1177/194589240401800607

10.1177/08959374970110011701

10.1016/j.tube.2010.10.001

10.1007/s11908-008-0064-1

10.1038/ismej.2011.83

10.1099/jmm.0.024083-0

10.1016/0195-6701(95)90062-4

10.1016/j.jhin.2003.09.020

10.1098/rstb.2007.2046

10.1128/AAC.01230-07

10.1128/AAC.01283-08

10.1038/ja.2011.58

10.1016/j.jcf.2008.06.009

10.1016/j.jcf.2005.05.018

10.1099/mic.0.27954-0

10.1002/(SICI)1099-0496(199909)28:3<159::AID-PPUL1>3.0.CO;2-1

10.1002/(SICI)1099-0496(199705)23:5<330::AID-PPUL4>3.0.CO;2-O

10.1002/(SICI)1099-0496(199603)21:3<153::AID-PPUL1>3.0.CO;2-R

10.1111/j.1600-0528.1991.tb00099.x

10.1080/08927014.2010.530347

10.1080/08927014.2010.542809

10.1046/j.1365-2958.1998.00797.x

10.1111/j.1699-0463.1990.tb01023.x

10.1128/IAI.73.4.2504-2514.2005

10.1111/j.1600-0463.2008.00018.x

10.1001/jama.287.13.1710

10.1128/IAI.00586-07

Rumbaugh KP, 2010, Biofilm Infections, 267

DigeI.Initial dental biofilm formation studied by confocal laser scanning microscopy and fluorescence in situ hybridization. PhD Thesis Denmark:Faculty of Health Sciences Aarhus University 2008.

10.1586/erm.09.81

10.1128/JCM.01650-10

10.1111/j.1574-695X.2010.00766.x

10.1038/nature05514

10.1034/j.1600-0706.2003.12254.x

10.1128/mBio.00199-10

10.1073/pnas.1018249108

10.1146/annurev.phyto.40.030402.110010

10.1128/AEM.67.10.4414-4425.2001

10.1073/pnas.92.10.4197

10.1155/2002/492656

10.1159/000259633

10.1111/j.1875-595X.2006.tb00107.x

10.1099/mic.0.26082-0

Marsh PD, 1991, Sugar, fluoride, pH and microbial homeostasis in dental plaque, Proc Finn Dent Soc, 87, 515

10.1086/377001

10.1007/s00266-009-9333-0

10.1016/j.tim.2004.11.010

10.1038/35101627

10.3109/17453670902947457

10.1056/NEJMoa061588

10.1161/CIRCULATIONAHA.109.906461

10.1007/s11999-008-0609-5

Kobayashi N, 2007, Brief ultrasonication improves detection of biofilm‐formative bacteria around a metal implant, Clin Orthop Relat Res, 457, 210, 10.1097/BLO.0b013e3180312042

10.1007/BF01640710

10.1097/BRS.0b013e3181c3b2f3

10.1016/S0966-842X(98)01425-5

10.1146/annurev.micro.57.030502.090720

10.1111/j.1462-5822.2009.01323.x

10.1128/IAI.00451-10

10.1128/IAI.00392-06

Wilson M, 2005, The Respiratory System and its Indigenous Microbiota. Microbial Inhabitants of Humans, 128

10.1128/jb.33.1.1-12.1937

10.1177/003591576505800503

10.1128/CMR.9.1.18

Evans AS, 1976, Causation and disease: the Henle‐Koch postulates revisited, Yale J Biol Med, 49, 175

Høiby N, 1977, Pseudomonas aeruginosa infection in cystic fibrosis. Diagnostic and prognostic significance of Pseudomonas aeruginosa precipitins determined by means of crossed immunoelectrophoresis, Scand J Respir Dis, 58, 65

Høiby N, 1975, Antibacterial precipitins and autoantibodies in serum of patients with cystic fibrosis, Scand J Respir Dis, 56, 38

10.1146/annurev.mi.40.100186.000333

10.1111/j.1699-0463.1993.tb00175.x

10.1183/1025448x.00035005

10.1111/j.1751-1097.2011.00962.x

10.1099/mic.0.032730-0

10.1016/S0140-6736(87)92286-0

10.1136/thx.2009.133082

10.1038/labinvest.3780024

10.1016/j.exer.2006.07.019

10.2337/diacare.28.2.461

LobmannR.Cytokine analyses in wound fluids of DFS: an objective reflection of inflammation and the state of healing.2005. DFSG annual meeting 2005 abstract number 07.

10.1152/ajplung.00492.2006

Dong Z, 2000, Membrane‐type matrix metalloproteinases in mice intracorneally infected with Pseudomonas aeruginosa, Invest Ophthalmol Vis Sci, 41, 4189

10.1016/S0022-3476(05)83478-X

10.1002/ppul.21198

10.1128/IAI.58.10.3363-3368.1990

10.1002/ppul.1950170107

10.1002/ppul.1950200204

10.1111/j.1651-2227.1988.tb10703.x

10.1016/j.jcf.2005.11.002

Pedersen SS, 1990, Immunoglobulin A and immunoglobulin G antibody responses to alginates from Pseudomonas aeruginosa in patients with cystic fibrosis, J Clin Microbiol, 28, 747, 10.1128/jcm.28.4.747-755.1990

10.1002/14651858.CD001127.pub2

10.1016/j.jcf.2004.09.001

10.1007/BF01712448

Kronborg G, 1992, Antibody responses to lipid A, core, and O sugars of the Pseudomonas aeruginosa lipopolysaccharide in chronically infected cystic fibrosis patients, J Clin Microbiol, 30, 1848, 10.1128/jcm.30.7.1848-1855.1992

Doring G, 1986, Elastase from polymorphonuclear leucocytes: a regulatory enzyme in immune complex disease, Clin Exp Immunol, 64, 597

10.1128/AAC.48.4.1175-1187.2004

10.1016/0140-6736(91)91446-2

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