The DOI matches its Crossref record; 11 of the 11 references it cites were found in a registry or an index.
The role of bacterial biofilms in chronic infections
Abstract
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 bridge in vitro and in vivo research 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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Without a proper diagnosis, clinicians may rely on systemic antibiotics, which are often ineffective against biofilm-associated bacteria due to their protective extracellular polymeric substance (EPS) matrix.4”
From SEMTWIST Quantification of Biofilm Infection in Human Chronic Wound Using Scanning Electron Microscopy and Machine Learning (2025) · cites this paper as [4]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The Environment and Disease: Association or Causation?
Hill, A. B. (1965) · Proceedings of the Royal Society of Medicine · doi:10.1177/003591576505800503 · Cited by 6,974
Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm
Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W., & Davies, D. G. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.4.1140-1154.2002 · Cited by 1,691
Socransky, S. S., & Haffajee, A. D. (2005) · Periodontology 2000 · doi:10.1111/j.1600-0757.2005.00107.x · Cited by 1,691
Are dental diseases examples of ecological catastrophes?
Marsh, P. D. (2003) · Microbiology · doi:10.1099/mic.0.26082-0 · Cited by 1,256
Mucus clearance as a primary innate defense mechanism for mammalian airways
Knowles, M. R., & Boucher, R. C. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0215217 · Cited by 1,054
Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation
Drenkard, E., & Ausubel, F. M. (2002) · Nature · doi:10.1038/416740a · Cited by 997
Microbial biofilms in the human gastrointestinal tract
Macfarlane, S., & Dillon, J. F. (2007) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2007.03287.x · Cited by 379 · cited 2×
“Macfarlane S, Dillon JF. Microbial biofilms in the human gastrointestinal tract.”
BackgroundMarrie, T. J., & Costerton, J. W. (1984) · Journal of Clinical Microbiology · doi:10.1128/jcm.19.5.687-693.1984 · Cited by 327
Price, L. B., Liu, C. M., Melendez, J. H., Frankel, Y. M., Engelthaler, D., Aziz, M., Bowers, J., Rattray, R., Ravel, J., Kingsley, C., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006462 · Cited by 237
Bacterial colonization and healing of venous leg ulcers
Madsen, S. M., Westh, H., Danielsen, L., & Rosdahl, V. T. (1996) · APMIS · doi:10.1111/j.1699-0463.1996.tb04955.x · Cited by 164
Research works printed but not linked: 369
- 10.1111/j.1574-695X.2010.00714.x · DOI
- Atlas RM, 1997, Microbial Ecology
- 10.1146/annurev.mi.49.100195.003431 · DOI
- 10.1289/ehp.98106a604 · DOI
- 10.1098/rstl.1684.0030 · DOI
- Henrici AT, 1933, Studies of freshwater bacteria, J Bacteriol, 25, 2132, 10.1128/jb.25.3.277-287.1933 · DOI
- HøibyN.Pseudomonas aeruginosa infection in cystic fibrosis.University of Copenhagen 1977. · DOI
- 10.1038/scientificamerican0178-86 · DOI
- 10.1139/m81-143 · DOI
- 10.1146/annurev.mi.41.100187.002251 · DOI · Paper page
- 10.1128/jb.176.8.2137-2142.1994 · DOI
- 10.1126/science.284.5418.1318 · DOI · Paper page
- 10.1007/978-3-540-68022-2_5 · DOI
- 10.1038/nrmicro1743 · DOI
- 10.1016/j.ijantimicag.2009.12.011 · DOI
- 10.1128/AAC.33.10.1824 · DOI
- 10.3201/eid0809.020063 · DOI · Paper page
- Zimmerli W, 2010, Biofilm Infections, 91
- 10.1016/S0140-6736(11)60988-4 · DOI
- 10.1177/1753465810368552 · DOI
- 10.1046/j.1365-2958.2003.03677.x · DOI
- 10.1046/j.1365-2958.2003.03525.x · DOI
- 10.1371/journal.pone.0027943 · DOI
- 10.1016/S0076-6879(99)10004-1 · DOI
- 10.1128/AEM.68.5.2495-2502.2002 · DOI
- 10.1111/j.1462-2920.2005.00775.x · DOI
- 10.1038/35023079 · DOI
- 10.1007/s00216-006-0774-x · DOI
- 10.1111/j.1365-2672.2007.03413.x · DOI
- 10.1172/JCI0213870 · DOI · Paper page
- 10.1136/thx.2009.114512 · DOI
- 10.1128/AAC.47.1.317-323.2003 · DOI
- Semmler AB, 1999, A re‐examination of twitching motility in Pseudomonas aeruginosa, Microbiology, 145, 2863, 10.1099/00221287-145-10-2863 · DOI
- 10.1146/annurev.micro.54.1.49 · DOI · Paper page
- 10.1186/gb-2003-4-6-219 · DOI
- 10.1128/AEM.68.9.4457-4464.2002 · DOI
- 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 · DOI
- 10.1017/S1479050505001699 · DOI
- 10.1186/1471-2180-10-294 · DOI
- 10.1128/JCM.43.10.5247-5255.2005 · DOI
- 10.1126/science.280.5361.295 · DOI · Paper page
- 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 · DOI
- 10.1146/annurev.micro.56.012302.160705 · DOI
- 10.1099/mic.0.27415-0 · DOI
- 10.1099/mic.0.26829-0 · DOI
- 10.1016/j.tim.2008.11.001 · DOI · Paper page
- 10.1371/journal.pone.0006289 · DOI
- 10.1128/AEM.67.12.5608-5613.2001 · DOI
- 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 · DOI
- 10.1128/JB.185.15.4585-4592.2003 · DOI
- 10.1111/j.1365-2958.2007.05772.x · DOI
- 10.1016/j.ahj.2003.09.018 · DOI
- 10.1046/j.1469-0691.2002.00427.x · DOI
- 10.1111/j.1574-6968.2004.tb09643.x · DOI
- 10.1046/j.1365-2958.2001.02337.x · DOI
- 10.1099/00221287-11-1-123 · DOI
- 10.1371/journal.ppat.1000354 · DOI
- 10.1111/j.1365-2958.2005.05008.x · DOI
- 10.1126/science.295.5559.1487 · DOI · Paper page
- 10.1371/journal.pone.0005822 · DOI
- 10.1073/pnas.0610226104 · DOI
- 10.1111/j.1365-2958.2009.06991.x · DOI
- 10.1046/j.1365-2958.2003.03833.x · DOI
- 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 · DOI
- 10.1128/JB.185.3.1027-1036.2003 · DOI
- 10.1128/JB.01515-06 · DOI
- 10.1186/1471-2180-5-30 · DOI
- 10.1111/j.1574-695X.2010.00690.x · DOI
- 10.1016/j.mib.2008.09.015 · DOI
- 10.1128/JB.00858-07 · DOI
- 10.1128/JB.183.3.1047-1057.2001 · DOI
- 10.1016/0891-5849(89)90078-6 · DOI
- 10.1111/j.1365-2672.1992.tb05009.x · DOI
- 10.1016/0014-5793(72)80685-9 · DOI
- 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 · DOI
- 10.1016/S1569-1993(02)00104-2 · DOI
- 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 · DOI
- 10.1086/431516 · DOI
- 10.1111/j.1365-2958.2009.06795.x · DOI
- 10.1016/j.mib.2007.09.010 · DOI
- 10.1111/j.1574-695X.2012.00956.x · DOI
- 10.1007/s00248-006-9063-7 · DOI
- 10.1093/jac/dkp165 · DOI
- 10.1371/journal.pone.0005724 · DOI
- 10.1128/JB.00257-06 · DOI
- 10.14219/jada.archive.2009.0049 · DOI
- 10.1038/nature08790 · DOI
- 10.1128/CMR.15.2.167-193.2002 · DOI · Paper page
- 10.1016/j.micinf.2003.08.009 · DOI
- 10.1128/AAC.48.4.1168-1174.2004 · DOI
- 10.1128/AAC.31.2.230 · DOI
- 10.1128/JB.183.18.5213-5222.2001 · DOI
- 10.1111/j.1348-0421.2004.tb03533.x · DOI
- 10.1098/rstb.2009.0037 · DOI
- 10.1111/j.1574-6976.2011.00295.x · DOI
- Giedraitiene A, 2011, Antibiotic resistance mechanisms of clinically important bacteria, Medicina (Kaunas), 47, 137
- 10.1111/j.1699-0463.1994.tb05219.x · DOI
- 10.1016/j.ajic.2006.05.219 · DOI
- 10.1371/journal.ppat.1000213 · DOI
- 10.1038/nrmicro1838 · DOI · Paper page
- 10.1128/AEM.70.10.6188-6196.2004 · DOI
- 10.1128/AEM.00710-08 · DOI
- Hoyle BD, 1991, Bacterial resistance to antibiotics: the role of biofilms, Prog Drug Res, 37, 91
- 10.1007/s11908-008-0006-y · DOI
- 10.1093/jac/22.6.777 · DOI
- 10.1093/jac/dkn462 · DOI
- 10.1128/AAC.48.1.48-52.2004 · DOI
- 10.1128/AAC.48.7.2659-2664.2004 · DOI
- 10.1128/AEM.69.4.2313-2320.2003 · DOI
- 10.1111/j.1365-2958.2008.06152.x · DOI
- 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 · DOI
- 10.1128/CMR.16.2.273-307.2003 · DOI
- 10.1016/S0065-2164(04)54007-8 · DOI
- 10.1007/s004230050196 · DOI
- 10.1128/IAI.70.11.6339-6345.2002 · DOI
- 10.1371/journal.pone.0002744 · DOI
- 10.1111/j.1462-2920.2004.00556.x · DOI · Paper page
- 10.1073/pnas.0505350102 · DOI
- 10.1164/ajrccm/140.6.1650 · DOI
- 10.1099/mic.0.031443-0 · DOI
- 10.1016/S0140-6736(01)05321-1 · DOI
- 10.1016/S1286-4579(00)01349-6 · DOI
- 10.1099/mic.0.27955-0 · DOI
- 10.1038/nrmicro1180 · DOI
- 10.1038/ismej.2008.47 · DOI
- 10.1128/JB.01581-07 · DOI
- 10.1128/jb.176.2.269-275.1994 · DOI
- Manefield M, 2002, Quorum sensing in context: out of molecular biology and into microbial ecology, Microbiology, 148, 3762, 10.1099/00221287-148-12-3762 · DOI
- 10.1093/molbev/msh097 · DOI
- 10.1038/208155a0 · DOI
- 10.1128/jb.104.1.313-322.1970 · DOI · Paper page
- 10.1111/j.1365-2958.1995.mmi_17020333.x · DOI
- 10.1093/emboj/cdg366 · DOI
- 10.1128/JB.185.7.2080-2095.2003 · DOI
- 10.1128/JB.185.7.2066-2079.2003 · DOI
- 10.1128/MMBR.56.4.662-676.1992 · DOI
- 10.1128/JB.187.5.1799-1814.2005 · DOI
- 10.1099/mic.0.27715-0 · DOI
- 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 · DOI
- 10.1073/pnas.92.14.6424 · DOI
- 10.1046/j.1365-2958.2001.02420.x · DOI
- 10.1093/jac/49.2.309 · DOI
- 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 · DOI
- 10.1046/j.1365-2958.1999.01672.x · DOI
- 10.1093/jac/dks002 · DOI
- 10.1146/annurev.genet.35.102401.090913 · DOI
- 10.1073/pnas.1934514100 · DOI
- 10.4161/cib.3.2.10429 · DOI
- 10.1073/pnas.052694299 · DOI
- 10.1046/j.1365-2672.2001.01339.x · DOI
- 10.1073/pnas.96.24.13904 · DOI
- 10.1128/JB.181.6.1703-1712.1999 · DOI
- 10.1111/j.1365-2958.1996.tb02495.x · DOI
- 10.1128/JB.182.21.5990-5996.2000 · DOI
- 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 · DOI
- 10.1016/0092-8674(94)90313-1 · DOI
- 10.1046/j.1365-2958.2003.03672.x · DOI
- 10.1016/j.ijmm.2006.01.038 · DOI
- 10.1016/j.mib.2009.01.005 · DOI
- 10.1172/JCI20195 · DOI
- 10.1128/IAI.68.5.2579-2586.2000 · DOI
- 10.1074/jbc.M109.031757 · DOI
- 10.3109/10408417709102809 · DOI
- 10.1038/scientificamerican0969-146 · DOI
- 10.1139/m77-249 · DOI
- 10.1007/s10126-007-9001-9 · DOI
- 10.1016/j.ijheh.2010.05.003 · DOI
- 10.1023/A:1020586312170 · DOI
- 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 · DOI
- 10.1128/AEM.65.11.5107-5116.1999 · DOI
- 10.1128/AEM.65.7.3182-3191.1999 · DOI
- 10.1128/AEM.62.5.1656-1663.1996 · DOI
- 10.1128/AEM.59.11.3840-3849.1993 · DOI
- 10.1111/j.1462-2920.2005.00973.x · DOI
- 10.1094/PHYTO.2002.92.12.1329 · DOI
- 10.1094/PHYTO.2004.94.11.1259 · DOI
- 10.1111/j.1574-6941.2008.00465.x · DOI
- Theilade E, 1970, Denal Plaque, 27
- 10.1902/jop.1975.46.1.10 · DOI
- 10.1128/JB.00983-08 · DOI
- 10.1128/AEM.72.4.2837-2848.2006 · DOI
- 10.1128/JB.185.11.3400-3409.2003 · DOI
- Nyvad B, 1993, Microbial colonization of human tooth surfaces, APMIS Suppl, 32, 1
- 10.1177/08959374940080022001 · DOI · Paper page
- 10.1159/000159604 · DOI
- 10.1128/MMBR.62.1.71-109.1998 · DOI
- 10.1099/mic.0.027706-0 · DOI · Paper page
- 10.1111/j.1600-0722.2007.00494.x · DOI
- 10.1126/science.1110591 · DOI · Paper page
- 10.1002/ibd.20176 · DOI
- 10.1097/00006454-200205000-00012 · DOI
- 10.1128/AEM.68.9.4225-4232.2002 · DOI
- 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 · DOI
- 10.1111/j.1440-1746.1993.tb01171.x · DOI
- 10.1155/2008/613979 · DOI
- 10.1111/j.1365-2133.1980.tb08139.x · DOI
200 of 369 shown
Cited by
Sorted by citations
Antibiotic resistance and persistence—implications for human health and treatment perspectives
Huemer, M., Mairpady Shambat, S., Brugger, S. D., & Zinkernagel, A. S. (2020) · The EMBO Reports · doi:10.15252/embr.202051034 · Cited by 850
Mixed‐species biofilm compromises wound healing by disrupting epidermal barrier function
Roy, S., Elgharably, H., Sinha, M., Ganesh, K., Chaney, S., Mann, E., Miller, C., Khanna, S., Bergdall, V. K., Powell, H. M., et al. (2014) · The Journal of Pathology · doi:10.1002/path.4360 · Cited by 208
“Host response to biofilm infection is typically chronic and governed by micro-environmental cues present at the site of infection [13].”
BackgroundYang, K. M., Kim, J.-S., Kim, H.-S., Kim, Y.-Y., Oh, J.-K., Jung, H.-W., Park, D.-S., & Bae, K.-H. (2021) · Scientific Reports · doi:10.1038/s41598-020-80921-x · Cited by 116
Selective pressures during chronic infection drive microbial competition and cooperation
Baishya, J., & Wakeman, C. A. (2019) · npj Biofilms and Microbiomes · doi:10.1038/s41522-019-0089-2 · Cited by 70
Singh, S., Muniz De Oliveira, F., Wang, C., Kumar, M., Xuan, Y., DeMazumder, D., Sen, C. K., & Roy, S. (2025) · Advances in Wound Care · doi:10.1089/wound.2024.0291 · Cited by 6
Metadata
- Authors
- Bjarnsholt, T.
- Venue
- APMIS
- Publisher
- Wiley
- Published
- 2013-05
- Volume
- 121
- Issue
- s136
- Pages
- 1-58
- ISSN
- 0903-4641
- 1600-0463
- Cited by
- 1,080
- References
- 11
- Language
- en
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review