SAGE Journals Online
Advertisement
Sign In to gain access to subscriptions and/or personal tools.

 

Advanced Search

Journal Navigation

Journal Home

Subscriptions

Archive

Contact Us

Table of Contents

Advertisement

Sign In to gain access to subscriptions and/or personal tools.
The International Journal of Lower Extremity Wounds
This Article
Right arrow Abstract Freely available
Right arrow Free Full Text (Free PDF) Free
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Request Reprints
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via Google Scholar
Right arrow Citing Articles via Scopus
Google Scholar
Right arrow Articles by Yager, D. R.
Right arrow Articles by Gilman, L. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Yager, D. R.
Right arrow Articles by Gilman, L. A.
Right arrowPubmed/NCBI databases
*Substance via MeSH
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?

Wound Fluids: A Window Into the Wound Environment?

Dorne R. Yager, PhD

Department of Surgery, Viginia Commonwealth University Medical Center, Richmond, Virginia, Department of Physiology, Virginia Commonweath University Medical Center, Richmond, Virginia, Department of Biochemistry, Virginia Commonwealth University Medical Center, Richmond, Virginia, dyager{at}vcu.edu

Robert A. Kulina, MS

Department of Surgery, Viginia Commonwealth University Medical Center, Richmond, Virginia

Laura A. Gilman, MS

Department of Surgery, Viginia Commonwealth University Medical Center, Richmond, Virginia

Wound healing of the skin is a complex biologic process involving temporal interactions between numerous types of cells, extracellular matrix molecules, and soluble factors. The process of repair can be viewed as involving 3 or 4 phases: homeostasis, inflammation, synthesis, and remodeling. These phases occur at different times and differ in their cellular, biochemical, and physiologic requirements. Disruption of one or more of these interactions can significantly interfere with the repair process. Such comorbidities as age, nutrition, immune status, and underlying disease status (eg, diabetes or venous stasis) contribute additional intricacy to the repair process. Because of this complexity, care of chronic wounds remains highly individualized, and it should not come as a surprise that treatment of these wounds as a group with single target therapies have met with only modest success. A major hurdle in the progression toward improved treatment regimens has been the lack of objective biochemical and physiological landmarks that can be used to assess wound status. Collection and biochemical characterization of wound fluids presents the opportunity to noninvasively obtain information reflecting the status of the wound and of specific biomarkers. This review discusses the collection of wound fluid and highlights biomarkers that may be useful to this end.

Key Words: wound fluid • chronic wound • biomarkers

References

  • Wysocki AB Wound fluids and the pathogenesis of chronic wounds. J Wound Ostomy Continence Nurs 1996;23:283-90.[Medline] [Order article via Infotrieve]
  • Mani R. Science of measurements in wound healing. Wound Repair Regen 1999;7:330-4.[CrossRef][Medline] [Order article via Infotrieve]
  • Trengove NJ, Langton SR, Stacey MC Biochemical analysis of wound fluid from nonhealing and healing chronic leg ulcers. Wound Repair Regen 1996;4:234-9.[CrossRef][Medline] [Order article via Infotrieve]
  • Barone EJ, Yager DR, Pozez AL, Olutoye OO, Crossland MC, Diegelmann RF, et al. Interleukin-1alpha and collagenase activity are elevated in chronic wounds. Plast Reconstr Surg 1998;102:1023-7.[Medline] [Order article via Infotrieve]
  • Grinnell F., Zhu M. Fibronectin degradation in chronic wounds depends on the relative levels of elastase, alpha1-proteinase inhibitor, and alpha2-macroglobulin. J Invest Dermatol 1996;106:335-41.[CrossRef][Medline] [Order article via Infotrieve]
  • Tarlton JF, Bailey AJ, Crawford E., Jones D., Moore K., Harding KD Prognostic value of markers of collagen remodeling in venous ulcers. Wound Repair Regen 1999;7:347-55.[CrossRef][Medline] [Order article via Infotrieve]
  • Trengove NJ, Stacey MC, Macauley S., Bennett N., Gibson J., Burslem F., et al. Analysis of the acute and chronic wound environments: the role of proteases and their inhibitors. Wound Repair Regen 1999;7:442-52.[CrossRef][Medline] [Order article via Infotrieve]
  • Yager DR, Zhang LY, Liang HX, Diegelmann RF, Cohen IK Wound fluids from human pressure ulcers contain elevated matrix metalloproteinase levels and activity compared to surgical wound fluids. J Invest Dermatol 1996;107:743-8.[CrossRef][Medline] [Order article via Infotrieve]
  • Baker EA, Leaper DJ Proteinases, their inhibitors, and cytokine profiles in acute wound fluid. Wound Repair Regen 2000;8:392-8.[CrossRef][Medline] [Order article via Infotrieve]
  • Nwomeh BC, Liang HX, Diegelmann RF, Cohen IK, Yager DR Dynamics of the matrix metalloproteinases MMP-1 and MMP-8 in acute open human dermal wounds. Wound Repair Regen 1998;6: 127-34.[CrossRef][Medline] [Order article via Infotrieve]
  • Nwomeh BC, Liang HX, Cohen IK, Yager DR MMP-8 is the predominant collagenase in healing wounds and nonhealing ulcers. J Surg Res 1999;81:189-95.[CrossRef][Medline] [Order article via Infotrieve]
  • Oono T., Fujiwara Y., Yoshioka T., Arata J. Prolidase activity in chronic wound and blister fluids. J Dermatol 1997;24:626-9.[Medline] [Order article via Infotrieve]
  • Ortega MR, Ganz T., Milner SM Human beta defensin is absent in burn blister fluid. Burns 2000;26:724-6.[CrossRef][Medline] [Order article via Infotrieve]
  • Wysocki AB, Grinnell F. Fibronectin profiles in normal and chronic wound fluid. Lab Invest 1990;63:825-31.[Medline] [Order article via Infotrieve]
  • Schilling JA, Favata BV, Radakovich M. Studies of fibroplasia in wound healing. Surg Gynecol Obstet 1953;96:143-9.[Medline] [Order article via Infotrieve]
  • Grotendorst GR, Martin GR, Pencev D., Sodek J., Harvey AK Stimulation of granulation tissue formation by platelet-derived growth factor in normal and diabetic rats. J Clin Invest 1985;76:2323-9.[Medline] [Order article via Infotrieve]
  • Robertson JG, Belford DA, Ballard FJ Clearance of IGFs and insulin from wounds: effect of IGF-binding protein interactions. Am J Physiol 1999;276:E663-71.[Medline] [Order article via Infotrieve]
  • James TJ, Hughes MA, Cherry GW, Taylor RP Simple biochemical markers to assess chronic wounds. Wound Repair Regen 2000;8:264-9.[CrossRef][Medline] [Order article via Infotrieve]
  • Mwaura B., Mahendran B., Hynes N., Defreitas D., Avalos G., Adegbola T., et al. The impact of differential expression of extracellular matrix metalloproteinase inducer, matrix metalloproteinase-2, tissue inhibitor of matrix metalloproteinase-2 and PDGF-AA on the chronicity of venous leg ulcers. Eur J Vasc Endovasc Surg 2006;31:306-10.[CrossRef][Medline] [Order article via Infotrieve]
  • Wallace HJ, Stacey MC Levels of tumor necrosis factor-alpha (TNFalpha) and soluble TNF receptors in chronic venous leg ulcers—correlations to healing status. J Invest Dermatol 1998;110:292-6.[CrossRef][Medline] [Order article via Infotrieve]
  • Yager DR, Chen SM, Ward SI, Olutoye OO, Diegelmann RF, Cohen IK Ability of chronic wound fluids to degrade peptide growth factors is associated with increased levels of elastase activity and diminished levels of proteinase inhibitors. Wound Repair Regen 1997;5:23-32.[CrossRef][Medline] [Order article via Infotrieve]
  • Trengove NJ, Bielefeldt-Ohmann H., Stacey MC Mitogenic activity and cytokine levels in non-healing and healing chronic leg ulcers. Wound Repair Regen 2000;8:13-25.[CrossRef][Medline] [Order article via Infotrieve]
  • Wysocki AB, Kusakabe AO, Chang S., Tuan TL Temporal expression of urokinase plasminogen activator, plasminogen activator inhibitor and gelatinase-B in chronic wound fluid switches from a chronic to acute wound profile with progression to healing. Wound Repair Regen 1999;7:154-65.[CrossRef][Medline] [Order article via Infotrieve]
  • Ladwig GP, Robson MC, Liu R., Kuhn MA, Muir DF, Schultz GS Ratios of activated matrix metalloproteinase-9 to tissue inhibitor of matrix metalloproteinase-1 in wound fluids are inversely correlated with healing of pressure ulcers. Wound Repair Regen 2002;10:26-37.[CrossRef][Medline] [Order article via Infotrieve]
  • Matsuoka J., Grotendorst GR Two peptides related to platelet-derived growth factor are present in human wound fluid. Proc Natl Acad Sci U S A 1989;86:4416-20.[Abstract/Free Full Text]
  • Cooper DM, Yu EZ, Hennessey P., Ko F., Robson MC Determination of endogenous cytokines in chronic wounds. Ann Surg 1994;219:688-91.[Medline] [Order article via Infotrieve]
  • Faria DT, Nickoloff BJ, Poverini PJ, Kunkel S., Burdick M., Strieter RM Chemokine and inflammatory cytokine changes during chronic wound healing. Wound Repair Regen 1997;5:310-22.[CrossRef][Medline] [Order article via Infotrieve]
  • Seah CC, Phillips TJ, Howard CE, Panova IP, Hayes CM, Asandra AS, et al. Chronic wound fluid suppresses proliferation of dermal fibroblasts through a Ras-mediated signaling pathway. J Invest Dermatol 2005;124:466-74.[CrossRef][Medline] [Order article via Infotrieve]
  • Schmidtchen A. Chronic ulcers: a method for sampling and analysis of wound fluid. Acta Derm Venereol 1999;79:291-5.[CrossRef][Medline] [Order article via Infotrieve]
  • Moseley R., Hilton JR, Waddington RJ, Harding KG, Stephens P., Thomas DW Comparison of oxidative stress biomarker profiles between acute and chronic wound environments. Wound Repair Regen 2004;12:419-29.[CrossRef][Medline] [Order article via Infotrieve]
  • Schmidtchen A. Degradation of antiproteinases, complement and fibronectin in chronic leg ulcers. Acta Derm Venereol 2000;80:179-84.[CrossRef][Medline] [Order article via Infotrieve]
  • Hoffman R., Noble J., Eagle M. The use of proteases as prognostic markers for the healing of venous leg ulcers. J Wound Care 1999;8:273-6.[Medline] [Order article via Infotrieve]
  • Simonsen L., Holstein P., Larsen K., Bulow J. Glucose metabolism in chronic diabetic foot ulcers measured in vivo using microdialysis. Clin Physiol 1998;18:355-9.[CrossRef][Medline] [Order article via Infotrieve]
  • Samuelsson A., Steinvall I., Sjoberg F. Microdialysis shows metabolic effects in skin during fluid resuscitation in burn-injured patients. Crit Care 2006;10:R172.[CrossRef][Medline] [Order article via Infotrieve]
  • Clough G., Noble M. Microdialysis—a model for studying chronic wounds. Int J Lower Extremity Wounds 2003;2:233-9.[CrossRef]
  • Clough GF Microdialysis of large molecules. AAPS J 2005;7:E686-92.[CrossRef][Medline] [Order article via Infotrieve]
  • Dealey C., Cameron J., Arrowsmith M. A study comparing two objective methods of quantifying the production of wound exudate. J Wound Care 2006;15:149-53.[Medline] [Order article via Infotrieve]
  • Stechmiller JK, Kilpadi DV, Childress B., Schultz GS Effect of Vacuum-Assisted Closure Therapy on the expression of cytokines and proteases in wound fluid of adults with pressure ulcers. Wound Repair Regen 2006;14:371-4.[CrossRef][Medline] [Order article via Infotrieve]
  • Greenburg GB, Hunt TK The proliferative response in vitro of vascular endothelial and smooth muscle cells exposed to wound fluids and macrophages. J Cell Physiol 1978;97:353-60.[CrossRef][Medline] [Order article via Infotrieve]
  • Katz MH, Alvarez AF, Kirsner RS, Eaglstein WH, Falanga V. Human wound fluid from acute wounds stimulates fibroblast and endothelial cell growth. J Am Acad Dermatol 1991;25:1054-8.[Medline] [Order article via Infotrieve]
  • Banda MJ, Knighton DR, Hunt TK, Werb Z. Isolation of a non-mitogenic angiogenesis factor from wound fluid. Proc Natl Acad Sci U S A 1982;79:7773-7.[Abstract/Free Full Text]
  • Bucalo B., Eaglstein WH, Falanga V. Inhibition of cell proliferation by chronic wound fluid. Wound Repair Regen 1993;1:181-6.[CrossRef][Medline] [Order article via Infotrieve]
  • Mendez MV, Raffetto JD, Phillips T., Menzoian JO, Park HY The proliferative capacity of neonatal skin fibroblasts is reduced after exposure to venous ulcer wound fluid: a potential mechanism for senescence in venous ulcers. J Vasc Surg 1999;30:734-43.[CrossRef][Medline] [Order article via Infotrieve]
  • Dinarello CA Differences between anti-tumor necrosis factor-alpha monoclonal antibodies and soluble TNF receptors in host defense impairment. J Rheumatol Suppl 2005;74:40-7.[Abstract/Free Full Text]
  • Streit M., Beleznay Z., Braathen LR Topical application of the tumour necrosis factor-alpha antibody infliximab improves healing of chronic wounds. Int Wound J 2006;3:171-9.[CrossRef][Medline] [Order article via Infotrieve]
  • Harris IR, Yee KC, Walters CE, Cunliffe WJ, Kearney JN, Wood EJ, et al. Cytokine and protease levels in healing and non-healing chronic venous leg ulcers. Exp Dermatol 1995;4:342-9.[CrossRef][Medline] [Order article via Infotrieve]
  • Galkowska H., Wojewodzka U., Olszewski WL Chemokines, cytokines, and growth factors in keratinocytes and dermal endothelial cells in the margin of chronic diabetic foot ulcers. Wound Repair Regen 2006;14:558-65.[CrossRef][Medline] [Order article via Infotrieve]
  • Cowin AJ, Hatzirodos N., Holding CA, Dunaiski V., Harries RH, Rayner TE, et al. Effect of healing on the expression of transforming growth factor beta(s) and their receptors in chronic venous leg ulcers. J Invest Dermatol 2001;117:1282-9.[CrossRef][Medline] [Order article via Infotrieve]
  • Higley HR, Ksander GA, Gerhardt CO, Falanga V. Extravasation of macromolecules and possible trapping of transforming growth factor-beta in venous ulceration. Br J Dermatol 1995; 132:79-85.[CrossRef][Medline] [Order article via Infotrieve]
  • Baxter CR Immunologic reactions in chronic wounds. Am J Surg 1994;167:12S-4S.[CrossRef][Medline] [Order article via Infotrieve]
  • James TJ, Hughes MA, Cherry GW, Taylor RP Evidence of oxidative stress in chronic venous ulcers. Wound Repair Regen 2003;11:172-6.[CrossRef][Medline] [Order article via Infotrieve]
  • Smith PC The causes of skin damage and leg ulceration in chronic venous disease. Int J Lower Extremity Wounds 2006;5: 160-8.[CrossRef]
  • Herrick SE, Sloan P., McGurk M., Freak L., McCollum CN, Ferguson MW Sequential changes in histologic pattern and extracellular matrix deposition during the healing of chronic venous ulcers. Am J Pathol 1992;141:1085-95.[Abstract]
  • Phillips TJ, Palko MJ, Bhawan J. Histologic evaluation of chronic human wounds treated with hydrocolloid and nonhydrocolloid dressings. J Am Acad Dermatol 1994;30:61-4.[Medline] [Order article via Infotrieve]
  • Dechert TA, Ducale AE, Ward SI, Yager DR Hyaluronan in human acute and chronic dermal wounds. Wound Repair Regen 2006;14:252-8.[CrossRef][Medline] [Order article via Infotrieve]
  • Mirastschijski U., Impola U., Jahkola T., Karlsmark T., AGren MS, Saarialho-Kere U. Ectopic localization of matrix metalloproteinase-9 in chronic cutaneous wounds. Hum Pathol 2002;33: 355-64.[CrossRef][Medline] [Order article via Infotrieve]
  • Weiss SJ Tissue destruction by neutrophils. N Engl J Med 1989;320:365-76.[Medline] [Order article via Infotrieve]
  • Parikh SV, de Lemos JA. Biomarkers in cardiovascular disease: integrating pathophysiology into clinical practice. Am J Med Sci 2006;332:186-97.[CrossRef][Medline] [Order article via Infotrieve]
  • Segura RM Useful clinical biological markers in diagnosis of pleural effusions in children. Paediatr Respir Rev 2004;5(Suppl A):S205-S212.[CrossRef][Medline] [Order article via Infotrieve]
  • Chua F., Laurent GJ Neutrophil elastase: mediator of extracellular matrix destruction and accumulation. Proc Am Thorac Soc 2006;3:424-7.[Abstract/Free Full Text]
  • Rao CN, Ladin DA, Liu YY, Chilukuri K., Hou ZZ, Woodley DT Alpha 1-antitrypsin is degraded and non-functional in chronic wounds but intact and functional in acute wounds: the inhibitor protects fibronectin from degradation by chronic wound fluid enzymes. J Invest Dermatol 1995;105:572-8.[CrossRef][Medline] [Order article via Infotrieve]
  • Wysocki AB, Staiano-Coico L., Grinnell F. Wound fluid from chronic leg ulcers contains elevated levels of metalloproteinases MMP-2 and MMP-9. J Invest Dermatol 1993;101:64-8.[CrossRef][Medline] [Order article via Infotrieve]
  • Nagase H., Woessner JF Jr. Matrix metalloproteinases. J Biol Chem 1999;274:21491-4.[Free Full Text]
  • Bullen EC, Longaker MT, Updike DL, Benton R., Ladin D., Hou Z., et al. Tissue inhibitor of metalloproteinases-1 is decreased and activated gelatinases are increased in chronic wounds. J Invest Dermatol 1995;104:236-40.[CrossRef][Medline] [Order article via Infotrieve]
  • Lobmann R., Ambrosch A., Schultz G., Waldmann K., Schiweck S., Lehnert H. Expression of matrix-metalloproteinases and their inhibitors in the wounds of diabetic and non-diabetic patients. Diabetologia 2002;45:1011-6.[CrossRef][Medline] [Order article via Infotrieve]
  • Weckroth M., Vaheri A., Lauharanta J., Sorsa T., Konttinen YT Matrix metalloproteinases, gelatinase and collagenase, in chronic leg ulcers. J Invest Dermatol 1996;106:1119-24.[CrossRef][Medline] [Order article via Infotrieve]
  • Vaalamo M., Mattila L., Johansson N., Kariniemi AL, Karjalainen-Lindsberg ML, Kahari VM, et al. Distinct populations of stromal cells express collagenase-3 (MMP-13) and collagenase-1 (MMP-1) in chronic ulcers but not in normally healing wounds. J Invest Dermatol 1997;109:96-101.[CrossRef][Medline] [Order article via Infotrieve]
  • Saarialho-Kere UK, Pentland AP, Birkedal-Hansen H., Parks WC, Welgus HG Distinct populations of basal keratinocytes express stromelysin-1 and stromelysin-2 in chronic wounds. J Clin Invest 1994;94:79-88.[Medline] [Order article via Infotrieve]
  • Rogers AA, Burnett S., Moore JC, Shakespeare PG Involvement of proteolytic enzymes—plasminogen activators and matrix metalloproteinases—in the pathophysiology of pressure ulcers. Wound Repair Regen 1995;3:273-83.[CrossRef][Medline] [Order article via Infotrieve]
  • Stacey MC, Burnand KG, Mahmoud-Alexandroni M., Gaffney PJ, Bhogal BS Tissue and urokinase plasminogen activators in the environs of venous and ischaemic leg ulcers. Br J Surg 1993;80:596-9.[CrossRef][Medline] [Order article via Infotrieve]
  • Pham CT Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 2006;6:541-50.[CrossRef][Medline] [Order article via Infotrieve]
  • Travis J., Salvesen GS Human plasma proteinase inhibitors. Annu Rev Biochem 1983;52:655-709.[CrossRef][Medline] [Order article via Infotrieve]
  • Mast AE, Enghild JJ, Nagase H., Suzuki K., Pizzo SV, Salvesen G. Kinetics and physiologic relevance of the inactivation of alpha 1-proteinase inhibitor, alpha 1-antichymotrypsin, and antithrombin III by matrix metalloproteinases-1 (tissue collagenase), -2 (72-kDa gelatinase/type IV collagenase), and -3 (stromelysin). J Biol Chem 1991;266:15810-6.[Abstract/Free Full Text]
  • Borregaard N. The respiratory burst of phagocytosis: biochemistry and subcellular localization. Immunol Lett 1985;11:165-71.[CrossRef][Medline] [Order article via Infotrieve]
  • Tauber AI, Babior BM Evidence for hydroxyl radical production by human neutrophils. J Clin Invest 1977;60:374-9.[Medline] [Order article via Infotrieve]
  • Reddy VY, Pizzo SV, Weiss SJ Functional inactivation and structural disruption of human alpha 2-macroglobulin by neutrophils and eosinophils. J Biol Chem 1989;264:13801-9.[Abstract/Free Full Text]
  • Ossanna PJ, Test ST, Matheson NR, Regiani S., Weiss SJ Oxidative regulation of neutrophil elastase-alpha-1-proteinase inhibitor interactions. J Clin Invest 1986;77:1939-51.[Medline] [Order article via Infotrieve]
  • Grootveld M., Halliwell B. Measurement of allantoin and uric acid in human body fluids. A potential index of free-radical reactions in vivo? Biochem J 1987;243:803-8.[Medline] [Order article via Infotrieve]
  • Morrow JD, Awad JA, Boss HJ, Blair IA, Roberts LJ Non-cyclooxygenase-derived prostanoids (F2-isoprostanes) are formed in situ on phospholipids. Proc Natl Acad Sci U S A 1992;89: 10721-5.[Abstract/Free Full Text]
  • Junger H., Sorkin LS Isoprostanes induce plasma extravasation in rat skin. Prostaglandins Other Lipid Mediat 2000;62:335-42.[CrossRef][Medline] [Order article via Infotrieve]
  • Yeoh-Ellerton S., Stacey MC Iron and 8-isoprostane levels in acute and chronic wounds. J Investig Dermatol 2003;121:918-25.[CrossRef][Medline] [Order article via Infotrieve]
  • Hall ED, Detloff MR, Johnson K., Kupina NC Peroxynitrite-mediated protein nitration and lipid peroxidation in a mouse model of traumatic brain injury. J Neurotrauma 2004;21:9-20.[CrossRef][Medline] [Order article via Infotrieve]
  • Chen LW, Wang JS, Chen HL, Chen JS, Hsu CM Peroxynitrite is an important mediator in thermal injury-induced lung damage. Crit Care Med 2003;31:2170-7.[CrossRef][Medline] [Order article via Infotrieve]
  • Kato Y., Uchida K., Kawakishi S. Oxidative fragmentation of collagen and prolyl peptide by Cu(II)/H2O2. Conversion of pro-line residue to 2-pyrrolidone. J Biol Chem 1992;267:23646-51.[Abstract/Free Full Text]
  • Rittie L., Monboisse JC, Gorisse MC, Gillery P. Malondialdehyde binding to proteins dramatically alters fibroblast functions. J Cell Physiol 2002;191:227-36.[CrossRef][Medline] [Order article via Infotrieve]
  • Maquart FX, Pasco S., Ramont L., Hornebeck W., Monboisse JC An introduction to matrikines: extracellular matrix-derived peptides which regulate cell activity. Implication in tumor invasion. Crit Rev Oncol Hematol 2004;49:199-202.[Medline] [Order article via Infotrieve]
  • Guo H., Li R., Zucker S., Toole BP EMMPRIN (CD147), an inducer of matrix metalloproteinase synthesis, also binds interstitial collagenase to the tumor cell surface. Cancer Res 2000;60:888-91.[Abstract/Free Full Text]
  • Tran KT, Griffith L., Wells A. Extracellular matrix signaling through growth factor receptors during wound healing. Wound Repair Regen 2004;12:262-8.[CrossRef][Medline] [Order article via Infotrieve]
  • Brassart B., Randoux A., Hornebeck W., Emonard H. Regulation of matrix metalloproteinase-2 (gelatinase A, MMP-2), membrane-type matrix metalloproteinase-1 (MT1-MMP) and tissue inhibitor of metalloproteinases-2 (TIMP-2) expression by elastin-derived peptides in human HT-1080 fibrosarcoma cell line. Clin Exp Metastasis 1998;16:489-500.[CrossRef][Medline] [Order article via Infotrieve]
  • Monboisse JC, Bellon G., Randoux A., Dufer J., Borel JP Activation of human neutrophils by type I collagen. Requirement of two different sequences. Biochem J 1990;270:459-62.[Medline] [Order article via Infotrieve]
  • Sweitzer SM, Fann SA, Borg TK, Baynes JW, Yost MJ What is the future of diabetic wound care? Diabetes Educ 2006;32:197-210.[Abstract/Free Full Text]
  • Turley EA, Noble PW, Bourguignon LY Signaling properties of hyaluronan receptors. J Biol Chem 2002;277:4589-92.[Free Full Text]
  • Jiang D., Liang J., Fan J., Yu S., Chen S., Luo Y., et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 2005;11:1173-9.[CrossRef][Medline] [Order article via Infotrieve]
  • McKee CM, Penno MB, Cowman M., Burdick MD, Strieter RM, Bao C., et al. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. J Clin Invest 1996;98:2403-13.[Medline] [Order article via Infotrieve]
  • McKee CM, Lowenstein CJ, Horton MR, Wu J., Bao C., Chin BY, et al. Hyaluronan fragments induce nitric-oxide synthase in murine macrophages through a nuclear factor kappaB-dependent mechanism. J Biol Chem 1997;272:8013-8.[Abstract/Free Full Text]
  • Agren UM, Tammi RH, Tammi MI Reactive oxygen species contribute to epidermal hyaluronan catabolism in human skin organ culture. Free Radic Biol Med 1997;23:996-1001.[CrossRef][Medline] [Order article via Infotrieve]
  • Moseley R., Waddington RJ, Embery G. Degradation of glycosaminoglycans by reactive oxygen species derived from stimulated polymorphonuclear leukocytes. Biochim Biophys Acta 1997;1362:221-31.[Medline] [Order article via Infotrieve]
  • Bendy RH, Nuccio PA, Wolfe E., Collins B., Tamburro C., Glass W., et al. Relationship of quantitative wound bacterial counts to healing of decubiti. Effect of topical gentamicin. Antimicrob Agents Chemother 1964;4:147-55.[Medline] [Order article via Infotrieve]
  • Robson MC, Heggers JP Delayed wound closure based on bacterial counts. J Surg Oncol 1970;2:379-83.[Medline] [Order article via Infotrieve]
  • Robson MC Wound infection. A failure of wound healing caused by an imbalance of bacteria. Surg Clin North Am 1997;77:637-50.[CrossRef][Medline] [Order article via Infotrieve]
  • Breidenbach WC, Trager S. Quantitative culture technique and infection in complex wounds of the extremities closed with free flaps. Plast Reconstr Surg 1995;95:860-5.[Medline] [Order article via Infotrieve]
  • Majewski W., Cybulski Z., Napierala M., Pukacki F., Staniszewski R., Pietkiewicz K., et al. The value of quantitative bacteriological investigations in the monitoring of treatment of ischaemic ulcerations of lower legs. Int Angiol 1995;14:381-4.[Medline] [Order article via Infotrieve]
  • Raahave D., Friis-Moller A., Bjerre-Jepsen K., Thiis-Knudsen J., Rasmussen LB The infective dose of aerobic and anaerobic bacteria in postoperative wound sepsis. Arch Surg 1986;121: 924-9.[Abstract/Free Full Text]
  • Trengove NJ, Stacey MC, McGechie DF, Mata S. Qualitative bacteriology and leg ulcer healing. J Wound Care 1996;5:277-80.[Medline] [Order article via Infotrieve]
  • Davies CE, Hill KE, Newcombe RG, Stephens P., Wilson MJ, Harding KG, et al. A prospective study of the microbiology of chronic venous leg ulcers to reevaluate the clinical predictive value of tissue biopsies and swabs. Wound Repair Regen 2007;15:17-22.[CrossRef][Medline] [Order article via Infotrieve]
  • Armstrong DG, Liswood PJ, Todd WF 1995 William J. Stickel Bronze Award. Prevalence of mixed infections in the diabetic pedal wound. A retrospective review of 112 infections. J Am Podiatr Med Assoc 1995;85:533-7.[Abstract]
  • Levine NS, Lindberg RB, Mason AD Jr, Pruitt BA Jr. The quantitative swab culture and smear: a quick, simple method for determining the number of viable aerobic bacteria on open wounds. J Trauma 1976;16:89-94.[Medline] [Order article via Infotrieve]

The International Journal of Lower Extremity Wounds, Vol. 6, No. 4, 262-272 (2007)
DOI: 10.1177/1534734607307035


Add to CiteULike CiteULike   Add to Complore Complore   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati   Add to Twitter Twitter    What's this?



This Article
Right arrow Abstract Freely available
Right arrow Free Full Text (Free PDF) Free
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Request Reprints
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via Google Scholar
Right arrow Citing Articles via Scopus
Google Scholar
Right arrow Articles by Yager, D. R.
Right arrow Articles by Gilman, L. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Yager, D. R.
Right arrow Articles by Gilman, L. A.
Right arrowPubmed/NCBI databases
*Substance via MeSH
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?

Advertisement