The DOI matches its Crossref record; 13 of the 13 references it cites were found in a registry or an index.
Bacterial colonization and healing of venous leg ulcers
Abstract
The aim of the study was to evaluate a possible influence of selected bacterial species on healing of venous leg ulcers. Fifty‐nine patients with venous leg ulcers were followed via frequent semiquantitative culture of bacteria from the ulcer surface and determination of the ulcer area over a period of 180 days. Occurrences of cellulitis were treated with systemic antibiotics. There was a significant difference in relative areas on days 90 and 180 when ulcers with growth of Pseudomonas aeruginosa were compared to those without (p=0.0080 and 0.0133, respectively). Ulcers with P. aeruginosa were characterized to a great extent by enlargement in contrast to those without. Ulcers with growth of Staphylococcus aureus or haemolytic streptococci healed significantly more slowly than those without when relative areas were compared on day 180 (p=0.0079 and 0.0492, respectively). Complete healing within the observation period of 180 days was observed in 10.5% of patients with P. aeruginosa and 35% of those without (p=0.0631), in 21.6% of patients with S. aureus and 62.5% of those without (p=0.0278), and in 10.5% of patients with haemolytic streptococci and 35% of those without (p = 0.0631). The initial areas of ulcers colonized with P. aeruginosa or 5. aureus were significantly larger than those without, but no significant correlation between initial areas and ulcer healing was revealed. Conclusion: Our results suggest that P. aeruginosa in venous leg ulcers can induce ulcer enlargement and/or cause a healing delay. The results also suggest a healing delay caused by 5. aureus and haemolytic streptococci. However, conclusions have to be treated with caution since P. aeruginosa was found in combination with haemolytic streptococci in 15.3% of the patients.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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
“wounds infected with Pseudomonas are slower to heal [31], [37], [38]”
From Interactions of Methicillin Resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in Polymicrobial Wound Infection (2013) · cites this paper as [38]
Citations
Cites
Hansson, C., Hoborn, J., Möller, A., & Swanbeck, G. (1995) · Acta Dermato Venereologica · doi:10.2340/00015555752430 · Cited by 197
Toxins of staphylococcus aureus
Freer, J. H., & ARBUTHNOTI, J. (1982) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(82)90042-0 · Cited by 159
THE EFFECT OF BACTERIAL COLONIZATION ON VENOUS ULCER HEALING
Halbert, A., Stacey, M. C., Rohr, J. B., & Jopp‐McKay, A. G. (1992) · Australasian Journal of Dermatology · doi:10.1111/j.1440-0960.1992.tb00083.x · Cited by 131
Bacteriology of Chronic Leg Ulcers
Lookingbill, D. P. (1978) · Archives of Dermatology · doi:10.1001/archderm.1978.01640240007002 · Cited by 124
Virulence Factors of Pseudomonas aeruginosa
D�ring, G., Maier, M., M�ller, E., Bibi, Z., T�mmler, B., & Kharazmi, A. (2015) · Antibiotics and chemotherapy/Antibiotica et chemotherapia · doi:10.1159/000414341 · Cited by 72
EPIDEMIOLOGY OF PSEUDOMONAS AERUGINOSA INFECTION IN PATIENTS TREATED AT A CYSTIC FIBROSIS CENTRE
Høiby, N., & Rosendal, K. (1980) · Acta Pathologica Microbiologica Scandinavica Section B Microbiology · doi:10.1111/j.1699-0463.1980.tb02617.x · Cited by 64
Pseudomonas aeruginosa Exotoxin A: Its Role in Retardation of Wound Healing The 1992 Lindberg Award
Heggers, J. P., Haydon, S., Ko, F., Hayward, P. G., & Robson, M. C. (1992) · Journal of Burn Care & Rehabilitation · doi:10.1097/00004630-199209000-00003 · Cited by 57
The significance of beta-haemolytic streptococci in chronic leg ulcers.
Schraibman, I. G. (1990) · PubMed · Cited by 51
Warburg, F. E., Danielsen, L., Madsen, S. M., Raaschou, H. O., Munkvad, S., Jensen, R., & Siersen, H. E. (1994) · Acta Dermato Venereologica · doi:10.2340/0001555574310311 · Cited by 44
Self-citationWannamaker, L. W. (1983) · Clinical Infectious Diseases · doi:10.1093/clinids/5.supplement_4.s723 · Cited by 44
Research works printed but not linked: 2
- Storey D. G., 1995, Comparison of Pseudomonas aeruginosa virulence factor expression to the clinical presentation of a pediatric population of cystic fibrosis patients, Pediatr. Pulmonol., A239
- Westh H., Cellulitis in chronic leg ulcers: Microbiology and influence of different local treatment regimes, In preparation
Cited by
Sorted by citations
Items 101–163 of 163
Benefits of maggot debridement therapy on leg ulcers: a literature review
Abela, G. (2017) · British Journal of Community Nursing · doi:10.12968/bjcn.2017.22.sup6.s14 · Cited by 23
Kroin, J. S., Li, J., Goldufsky, J. W., Gupta, K. H., Moghtaderi, M., Buvanendran, A., & Shafikhani, S. H. (2016) · Journal of Medical Microbiology · doi:10.1099/jmm.0.000295 · Cited by 22
“aeruginosa accounts for ~25% of SSIs, and its presence in wound correlates with a poor prognosis for healing (Halbert et al., 1992; Madsen et al., 1996; Giacometti et al., 2000; Winstanley et al., 2005; Gjødsbøl et al., 2006; Ramakant et al., 2011; Malik et al., 2013).”
BackgroundDanielsen, L., Balslev, E., Döring, G., Høiby, N., Madsen, S. M., Ågren, M. S., Thomsen, H. K., FOS, H. H. S., & Westh, H. (1998) · Apmis · doi:10.1111/j.1699-0463.1998.tb00218.x · Cited by 22
Self-citationEcthyma-Gangrenosum-Like Bullous Pemphigoid
Steiner, J. G., Trüeb, R. M., Kerl, K., Mühleisen, B., French, L. E., & Hofbauer, G. F. L. (2010) · Dermatology · doi:10.1159/000316098 · Cited by 20
Thomson, P. D. (1998) · Journal of Wound Care · doi:10.12968/jowc.1998.7.9.477 · Cited by 20
The effect of bacteria on leg ulcer healing
Harker, J. (2001) · British Journal of Community Nursing · doi:10.12968/bjcn.2001.6.3.7100 · Cited by 19
Phalak, P., & Henson, M. A. (2019) · Journal of Applied Microbiology · doi:10.1111/jam.14421 · Cited by 20
“These predictions are supported by studies showing that the presence of Pseudomonas along with Staphylococcus generates larger chronic wounds and delays/prevents the healing process (Madsen et al. 1996; Gjødsbøl et al. 2006; Kirketerp-Møller et al. 2008).”
ResultOkamoto, S., Ogai, K., Mukai, K., & Sugama, J. (2021) · Microorganisms · doi:10.3390/microorganisms9081603 · Cited by 19
Forlee, M. V., Rossington, A., & Searle, R. J. (2014) · International Wound Journal · doi:10.1111/iwj.12239 · Cited by 15
“Other studies have shown associations between delays in healing correlated with the presence of bacterial species (19,20).”
BackgroundGerner, E., Almqvist, S., Werthén, M., & Trobos, M. (2020) · Journal of Medical Microbiology · doi:10.1099/jmm.0.001188 · Cited by 17
Karnik, T., Dempsey, S. G., Jerram, M. J., Nagarajan, A. P., Rajam, R., May, B. C. H., & Miller, C. H. (2019) · Biomaterials Research · doi:10.1186/s40824-019-0155-0 · Cited by 14
Eisenbeis, J., Peisker, H., Backes, C. S., Bur, S., Hölters, S., Thewes, N., Greiner, M., Junker, C., Schwarz, E. C., Hoth, M., et al. (2017) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2017.01.002 · Cited by 15
A charcoal dressing with silver in wound infection: clinical evidence
White, R. J. (2001) · British Journal of Community Nursing · doi:10.12968/bjcn.2001.6.sup3.12621 · Cited by 14
Aerobic bacterial isolates from infected wounds
Esebelahie, N., Newton-Esebelahie, F., & Omoregie, R. (2013) · African Journal of Clinical and Experimental Microbiology · doi:10.4314/ajcem.v14i3.6 · Cited by 13
“Although the majority of wounds are polymicrobial involving both aerobes and anaerobes, aerobic pathogens such as Staphylococcus aureus, Pseudomonas aeroginosa, and beta haemolytic Streptococci have been most frequently reported as the cause of delay wound healing (6-9, 3).”
BackgroundTreatment Options for Venous Leg Ulcers
Thakral, G., Fontaine, J. L., Kim, P. J., Najafi, B., Nichols, A., & Lavery, L. A. (2015) · Advances in Skin & Wound Care · doi:10.1097/01.asw.0000462328.60670.c3 · Cited by 13
SOCIEDAD ARGENTINA DE DERMATOLOGÍA
Marini, M., General, S., Valdez, R., Científico, S., Stringa, O., Díaz, R. G., Actas, S. D., Ubogui, J., Woscoff, A., Jaimovich, L., et al. (2008) · Cited by 12
Lantis, J. C., & Gendics, C. (2011) · Journal of Wound Care · doi:10.12968/jowc.2011.20.2.90 · Cited by 11
Salmon cartilage proteoglycan promotes the healing process of Staphylococcus aureus-infected wound
Hirose, S., Narita, K., Asano, K., & Nakane, A. (2018) · Heliyon · doi:10.1016/j.heliyon.2018.e00587 · Cited by 11
Kintarak, S., Nair, S. P., Speight, P. M., & Whawell, S. A. (2004) · Archives of Dermatological Research · doi:10.1007/s00403-004-0515-y · Cited by 11
“The presence of Staphylococcus aureus in wound infections is common and is thought to delay healing and increase the risk of death in immunocompromised patients [3, 4].”
BackgroundRisk Factors for Unsuccessful Treatment and Complications With Negative Pressure Wound Therapy
Fagerdahl, A., Boström, L., Ulfvarson, J., & Ottosson, C. (2012) · Cited by 11
Xu, L., Wang, H.-X., & Zhao, L. (2019) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2019.101425 · Cited by 10
Hussein, Y. A., & Luti, K. J. K. (2020) · Iraqi Journal of Science · doi:10.24996/ijs.2020.61.8.10 · Cited by 9
“[7] reported that chronic wounds are colonized by various bacterial populations, which contribute directly and indirectly to chronic phenotypes of wounds.”
BackgroundRocasalbas, G., Touriño, S., Torres, J. L., & Tzanov, T. (2013) · Journal of Materials Chemistry B · doi:10.1039/c2tb00239f · Cited by 9
RAMELET, A. A., & Perrenoud, D. (1999) · KARGER eBooks · doi:10.1159/000060632 · Cited by 8
Immunomodulatory properties of medicinal maggots Lucilia sericata in wound healing process
Bohová, J., Majtán, J., & Takáč, P. (2012) · TANG [HUMANITAS MEDICINE] · doi:10.5667/tang.2012.0025 · Cited by 7
Żmudzińska, M., Czarnecka-Operacz, M. M., & Silny, W. (2005) · PubMed · Cited by 6
Bacterial colonization of leg ulcers and its effect on success rate of skin grafting
Balaji, D. K., Bhaskarla, V. V. R., & Sadakshy (2020) · International Surgery Journal · doi:10.18203/2349-2902.isj20205357 · Cited by 6
“Madsen et al did a study on 59 venous ulcers to evaluate the possible influence of selected bacterial species on healing of leg ulcers.(20) In their study they followed up the patients for 180 days.”
BackgroundNorman, G., Dumville, J. C., Mohapatra, D. P., Hassan, I. A., Edwards, J., & Christie, J. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd011821 · Cited by 6
Stewart, P. S., Kim, J., James, G. A., Yi, F., Stechmiller, J. K., Weaver, M. T., Kelly, D. L., Fisher, S. T., Schultz, G. S., & Lyon, D. (2024) · Wound Repair and Regeneration · doi:10.1111/wrr.13230 · Cited by 5
“Although many studies have not found an association of wound healing and the presence of certain bacterial species, the presence of Pseudomonas aeruginosa was associated with poor healing outcomes in both culture-based 58,59 and culture-independent 60 studies.”
Quand s’inquiéter devant un ulcère de jambe d’origine vasculaire ?
Lazareth, I. (2016) · Journal des Maladies Vasculaires · doi:10.1016/j.jmv.2016.07.008 · Cited by 5
“[2] Madsen SM, Westh H, Danielsen L, Rosdahl VT.”
BackgroundEffect ofPseudomonascolonisation on lower limb venous ulcer healing: a systematic review
Toale, C., Kelly, A., Leahy, F. C., Meagher, H., Stapleton, P. J., Moloney, M. A., & Kavanagh, E. G. (2022) · Journal of Wound Care · doi:10.12968/jowc.2022.31.2.186 · Cited by 5
Prevalence analysis of fungi in chronic lower extremity ulcers .
Foroozan, M., Contet‐Audonneau, N., Granel‐Brocard, F., Barbaud, A. M., & Schmutz, J. ‐. (2011) · PubMed · Cited by 5
Infection in Diabetes: Epidemiology, Immune Dysfunctions, and Therapeutics
Roy, R., Singh, R. K., & Shafikhani, S. H. (2024) · Contemporary diabetes · doi:10.1007/978-3-031-55715-6_17 · Cited by 4
Oropallo, A., Lee, P. J., Rao, A. S., & Gray, M. D. (2025) · Journal of Vascular Surgery Venous and Lymphatic Disorders · doi:10.1016/j.jvsv.2025.102213 · Cited by 4
“11,18,19 Bio fi lms have an extracellular matrix that triggers the activation of macrophages and neutrophils.”
Arfaoui-Elhif, R., Pochat‐Bohatier, C., Bechelany, M., Tekfa, M. I. B., Ortiz, D. G., Miele, P., Romdhane, M. R. B., & Srasra, E. (2023) · Colloids and Surfaces A Physicochemical and Engineering Aspects · doi:10.1016/j.colsurfa.2023.132421 · Cited by 4
Chronic wounds and adaptive Pseudomonas aeruginosa: A phenotypic and genotypic characterization
Buchholtz, K., Jønsson, R., Marvig, R. L., Mojsoska, B., & Krogfelt, K. A. (2025) · Current Research in Microbial Sciences · doi:10.1016/j.crmicr.2025.100348 · Cited by 4
“…patients as they heal very slowly, and in venous leg ulcers are seen to be larger in size and associated with more severe wound outcomes compared to wounds where the pathogen is not present (Halbert et al., 1992; Madsen et al., 1996; Kirketerp-M ø ller et al., 2008; Gj ø dsb ø l et al., 2006).”
Mirzaei, Y., Hagemeister, K., Hüffel, M., Schwandt, T., Tolba, R. H., & Steitz, J. (2022) · BioMed Research International · doi:10.1155/2022/3483238 · Cited by 4
Antibiotics, Antiseptics, and Cutaneous Ulcers
(2005) · Springer eBooks · doi:10.1007/3-540-26761-1_10 · Cited by 4
Do Commonly Used Antimicrobial Topicals Facilitate Venous Leg Ulcer Healing?
Alihosseini, C., Kopelman, H., Lam, J., & Phillips, T. J. (2023) · Advances in Skin & Wound Care · doi:10.1097/01.asw.0000926636.51805.d5 · Cited by 4
“Most Common Microbial Colonizers of VLUs Tissue cultures from VLU biopsies tend to indicate that Staphylococcus aureus and Pseudomonas aeruginosa are the most frequent colonizers of VLUs, although some studies have found that Escherichia coli ismore common.(5,6) Swabs and studies using peptide nucleic acid fluorescenc…”
ResultMan, E., & Hoskins, C. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-90514-5.00019-5 · Cited by 3
A Systematic Review on Antimicrobial Applications of Nanofibres
Patil, M. L., Gaikwad, S. S., & Kapare, H. S. (2024) · Research Journal of Pharmacy and Technology · doi:10.52711/0974-360x.2024.00067 · Cited by 3
10 praxisnahe Tipps zur Behandlung chronischer Wunden
Erfurt-Berge, C. S., & Renner, R. (2014) · Aktuelle Dermatologie · doi:10.1055/s-0034-1365806 · Cited by 3
Abbas, O. L., Borman, H., Bahar, T., Ertaş, N. M., & Haberal, M. A. (2014) · Journal of Burn Care & Research · doi:10.1097/bcr.0000000000000072 · Cited by 3
Cellulitis in Venous Leg Ulcers Treated with a Hydrocolloid Dressing
Westh, H., Warburg, F. E., Madsen, S., Larsen, S. O., & Danielsen, L. (1998) · Phlebology The Journal of Venous Disease · doi:10.1177/026835559801300208 · Cited by 3
Self-citationDry wound healing concept using spray-on dressings for chronic wounds
Jolly, S., & Jolly, S. (2011) · Elsevier eBooks · doi:10.1533/9780857093301.2.209 · Cited by 3
Pham, E., Reynolds, L., Navarro, S., Hamood, A. N., Jones-Donaldson, L. M., & Smith, A. C. (2024) · Diagnostics · doi:10.3390/diagnostics14141474 · Cited by 2
“Chronic wounds harboring P. aeruginosa are often larger and experience longer duration than wounds without P. aeruginosa [14,25,28–30], leading to worse patient outcomes.”
BackgroundPrognostic factors for delayed healing of venous leg ulcers
Simka, M. (2014) · Phlebological Review · doi:10.5114/pr.2014.48906 · Cited by 2
“Other researchers also confirmed a deleterious role of several bacterial species resulting in poor healing: Pseudomonas aeruginosa [19, 34, 35], Staphylococcus aureus [19, 21, 33, 34], anaerobes [33], and β-haemolytic streptococci [33, 35].”
Chronic Leg Ulcer Presenting Through Emergency Surgical Unit
(2007) · The Internet Journal of Surgery · doi:10.5580/1051 · Cited by 2
Thaarup, I. C., & Bjarnsholt, T. (2023) · Springer eBooks · doi:10.1007/978-3-031-26110-7_10 · Cited by 1
Prevention of Biofilm Infections
Oh, K., & Kim, K.-K. (2009) · Journal of Bacteriology and Virology · doi:10.4167/jbv.2009.39.4.237 · Cited by 2
Sensors for Detecting and Combating Wound Infection
Davis, J., & McLister, A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803762-1.00006-0 · Cited by 1
Petz, F. D. F. C., Méier, M. J., Roehrs, H., & Pott, F. S. (2018) · The JBI Database of Systematic Reviews and Implementation Reports · doi:10.11124/jbisrir-2017-003400 · Cited by 1
Biopelículas bacterianas en heridas crónicas
Gómez, C. C. B., García-Aristizabal, M. P., Yeisson David Reyes, M., & Huertas, M. G. (2019) · Revista Salud Bosque · doi:10.18270/rsb.v9i1.2643 · Cited by 2
Rosolen, S. G., Multari, D., Woods, M., & Jongh, O. (2009) · Elsevier eBooks · doi:10.1016/b978-070202861-8.50007-5 · Cited by 1
Implications of Biofilm Formation in Chronic Wounds and in Cystic Fibrosis
Shunmugaperumal, T. (2010) · Wiley eBooks · doi:10.1002/9780470640463.ch8
Ecology of Biofilms in Chronic Wounds
Bjarnsholt, T., & Givskov, M. (2010) · Research at the University of Copenhagen (University of Copenhagen)
The role of mast cells in the immune response against bacterial infections
Zimmermann, C. (2016) · DepositOnce · doi:10.14279/depositonce-5528
“aeruginosa-infected wounds compared to 35% of non-infected wounds (186).”
BackgroundMicrobial Bioburden in Venous Leg Ulcers
Tuttle, M. S. (2014) · OhioLink ETD Center (Ohio Library and Information Network)
specialists., T. G. I. A. D. W. R. A. M. I. S. T. D. P. I. W. T. O. T. (. H. A. P. O. R. O. T. P. I. C. T. G. I. B. O. T. R. O. S. R. A. C. O. A. A. E. G. M. P. T. D. I. I. A. A. G. F. T. E. D. A. T. O. V. L. U. B. D. O. O. M. (2016) · Journal of the European Academy of Dermatology and Venereology · doi:10.1111/jdv.3_13848
Ozşen, K. (2022) · Cardiovascular Perfusion and Nursing · doi:10.5606/e-cvpn.2022.198
Evaluation of some immunological parameters associated with wound infection
Hameed, S. F., & Salim, D. K. (2026) · AIP conference proceedings · doi:10.1063/5.0324261
Roberts, B., Laxton, C. S., Spencer, D. L., Thaarup, I. C., Heeb, S., Penfold, C. N., & Hardie, K. R. (2026) · Microbiology · doi:10.1099/mic.0.001719
“The prevalence of P. aeruginosa within a wound is linked to prognosis, as the presence of the bacterium is associated with more severe and clinically persistent infections and prolonged healing times [7, 8].”
Development of multifunctional biopolymeric materials for teatment of decubitus ulcers
Lozano, G. R. (2012) · UPCommons institutional repository (Universitat Politècnica de Catalunya) · doi:10.5821/dissertation-2117-94829
“aeruginosa were larger than those that did not, and the healing process also seemed to be more severely hindered for those wounds [105, 106, 109].”
Background
Metadata
- Authors
- Madsen, S. M., Westh, H., Danielsen, L., & Rosdahl, V. T.
- Affiliations
- Bispebjerg Hospital (DK)
- Statens Serum Institut (DK)
- Corresponding author
- Danielsen, Lis
- ORCID
- Westh, Henrik
- Venue
- APMIS
- Publisher
- Wiley
- Published
- 1996-07-08
- Volume
- 104
- Issue
- 7-8
- Pages
- 895-899
- ISSN
- 0903-4641 (ISSN-L)
- 1600-0463
- OpenAlex
- W1990659092
- Cited by
- 164
- References
- 13
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 5 · 2023: 6 · 2022: 6 · 2021: 4 · 2020: 8 · 2019: 6 · 2018: 3 · 2017: 5 · 2016: 13 · 2015: 8 · 2014: 16 · 2013: 15 · 2012: 7
- FWCI
- 4.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Apmis (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Surgery › Wound Healing and Treatments
- Health Sciences › Medicine › Surgery › Diagnosis and Treatment of Venous Diseases
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetic Foot Ulcer Assessment and Management
- Keywords
- venous leg ulcers, bacterial colonization, ulcer healing, Pseudomonas aeruginosa, Staphylococcus aureus, hemolytic streptococci, cellulitis, wound infection
- MeSH terms
- Bacterial Infections, Cellulitis, Humans, Pseudomonas Infections, Staphylococcal Infections, Streptococcal Infections, Varicose Ulcer, Wound Healing
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
