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Corticosteroids and Wound Healing: Clinical Considerations in the Perioperative Period

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Corticosteroids and Wound Healing: Clinical Considerations in the Perioperative Period The American Journal of Surgery (2013) 206, 410-417 Review Corticosteroids and wound healing: clinical considerations in the perioperative period Audrey S. Wang, M.D.a,*, Ehrin J. Armstrong, M.D., M.Sc.b, April W. Armstrong, M.D., M.P.H.a aDepartment of Dermatology, University of California, Davis, 3301 C Street, Suite 1400, Sacramento, CA 95816; bDepartment of Internal Medicine, Division of Cardiovascular Medicine, University of California, Davis, 4860 Y Street, Suite 2820, Sacramento, CA 95817 KEYWORDS: Abstract Corticosteroids; BACKGROUND: Determining whether systemic corticosteroids impair wound healing is a clinically Wound healing; relevant topic that has important management implications. Perioperative METHODS: We reviewed literature on the effects of corticosteroids on wound healing from animal and human studies searching MEDLINE from 1949 to 2011. RESULTS: Some animal studies show a 30% reduction in wound tensile strength with perioperative corticosteroids at 15 to 40 mg/kg/day. The preponderance of human literature found that high-dose cor- ticosteroid administration for ,10 days has no clinically important effect on wound healing. In patients taking chronic corticosteroids for at least 30 days before surgery, their rates of wound complications may be increased 2 to 5 times compared with those not taking corticosteroids. Complication rates may vary depending on dose and duration of steroid use, comorbidities, and types of surgery. CONCLUSIONS: Acute, high-dose systemic corticosteroid use likely has no clinically significant effect on wound healing, whereas chronic systemic steroids may impair wound healing in susceptible individuals. Ó 2013 Elsevier Inc. All rights reserved. The effects of corticosteroids on wound healing have perioperative corticosteroid administration, namely, dosing, been a topic of great interest among surgeons, internists, and chronicity, and timing relative to surgery. dermatologists. Within the past century, pivotal discoveries In 1949, Hench et al12 revolutionized the treatment in the mechanisms of wound healing have enhanced our of rheumatologic patients when they reported dramatic understanding of the molecular interactions between corti- improvement of rheumatoid arthritis symptoms in pati- costeroids and cutaneous wounds.1–11 These basic science ents treated with 50 to 100 mg of 17-hydroxy-11- discoveries, coupled with findings from clinical studies, dehydrocorticosterone daily. The following year, they have highlighted several important considerations regarding were awarded the Nobel Prize in Medicine for this ‘‘medi- cal miracle.’’ Since then, systemic corticosteroids have been used to treat various inflammatory conditions, includ- This work was not supported by any funding sources. The authors ing rheumatoid arthritis, temporal arteritis, gout, and in- declare no conflicts of interest. flammatory bowel disease, which may require surgical * Corresponding author. management. E-mail address: [email protected] 12 Manuscript received June 25, 2012; revised manuscript November 1, Importantly, the initial report from Hench et al did not 2012 describe wound healing concerns, but subsequent clinical 0002-9610/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.amjsurg.2012.11.018 A.S. Wang et al. Corticosteroids and wound healing 411 reports noted potential adverse effects of corticosteroids on tissue and may thereby decrease the chemotactic and mito- wound healing.13 Later studies in animal models also genic stimulus for other inflammatory cells.1,8 Dexametha- showed corticosteroid-induced wound healing impairment sone also downregulates endothelial cell expression of at high doses.14–27 Thus, when patients on systemic cortico- intercellular adhesion molecule 1 (ICAM-1) in culture and steroids require surgical procedures, concerns may arise re- in healing colonic anastomoses, resulting in attenuated gran- garding postoperative wound complications. ulocyte adhesion and migration.4,11 Consistent with this This article reviews the three aspects of the effects of finding, high-dose corticosteroids reduce the extent of mac- corticosteroids on wound healing. First, the mechanisms of rophage infiltration into the wound.9 normal wound healing will be summarized, followed by an overview of the molecular interactions between corticoste- Proliferative phase. Platelets and macrophages from the roids and the wound healing process in the context of a inflammatory phase establish the growth factor and cyto- cutaneous wound. Second, data regarding the effects of kine milieu that drives angiogenesis, fibroplasia, and re- 32 corticosteroids on wound healing in animal models and epithelialization during the proliferative phase. Following humans will be presented. Finally, dosing, chronicity, and construction of the framework of extracellular matrix and timing of corticosteroid administration relative to surgery new blood vessels, epithelial cells from the basal layer 35,36 will be discussed. migrate across the basal lamina. Re-epithelialization, stimulated by keratinocyte growth factor (KGF),37 is also Corticosteroid structure and function dependent upon plasmin and matrix metalloproteinases to digest the leading edge of the fibrin clot.38 Corticosteroids reduce TGF-ß levels and mesenchymal cell expression of Corticosteroids are lipophilic molecules derived from keratinocyte growth factor (KGF), which attenuates fibro- the endogenous hormone cortisol that diffuse into cells, blast proliferation5 and impairs wound re-epithelialization.2 then bind to and activate glucocorticoid receptors (GRs). Activated GRs dimerize and diffuse into the nucleus, where Remodeling phase. During remodeling, the wound un- they drive or inhibit gene transcription by binding to gluco- dergoes contraction and alters its collagen expression corticoid response elements present in the promoter re- pattern. Myofibroblasts facilitate wound contraction via gions of target genes. Structural alterations of the cortisol TGF-ß1 stimulation.39,40 Collagen remodeling requires col- backbone result in corticosteroids with varying tissue distri- lagen digestion and a switch from type III collagen in the 28 bution, rate of hepatic metabolism, and affinity for the GR. wound to type I collagen.3,10 Animal studies suggest that corticosteroids impair collagen turnover,3,10 disrupt der- Molecular mechanisms of corticosteroids and mal–epidermal junctional interactions,7 and decrease the their effects on wound healing tensile strength of cutaneous wounds by reducing collagen accumulation.6,41 Corticosteroids have been shown to affect all major steps Notably, the mechanisms described above occur in the of the wound healing process,29,30 which is somewhat arbi- setting of acute wound healing, but corticosteroids have trarily divided into 3 phases: inflammatory, proliferative, systemic and possibly indirect effects as well, which are and remodeling. In reality, these 3 phases overlap signifi- less well understood. Insights into these processes could cantly, and signaling cascades initiated in 1 phase influence promise new therapeutics, including steroids that retain cell growth and differentiation in later phases.31 anti-inflammatory properties but have minimal adverse effects on wound healing. Inflammatory phase. Immediately after wounding, plate- lets and the coagulation cascade initiate primary and Clinical effects of corticosteroids on wound secondary hemostasis. During primary hemostasis, platelets healing release numerous cytokines, including transforming growth factor-ß (TGF-ß), which trigger the subsequent production In the same year that Hench et al12 described their of additional growth factors, such as basic fibroblast growth ‘‘medical miracle,’’ Ragan et al13 documented impaired factor 2, from nearby cells. The fibrin mesh scaffold wound healing in 3 of 8 rheumatoid arthritis patients treated established during secondary hemostasis acts as a reservoir with 25 U/day of adrenocorticotropic hormone (roughly for growth factors and provides a matrix for future tissue equivalent to 75 mg/day of prednisone). Specifically, these deposition.32 In addition, cellular membrane-bound recep- patients developed a nonhealing biopsy site, a nonhealing tors, such as intercellular adhesion molecule 1 (ICAM-1), fa- episiotomy site and decubitus ulcer, and nonhealing abscess cilitate recruitment of inflammatory cells.33 Within minutes drainage sites. In 2 of these patients, the wounds quickly of injury, neutrophils arrive.34 Then, over the course of 2 to 3 granulated within 4 days of discontinuing adrenocorticotro- days, macrophages become predominant.9 Treatment with pic hormone treatment. These findings led to subsequent the corticosteroid dexamethasone decreases the expression studies to better evaluate the effects of corticosteroids on of cytokines, including TGF-b1, platelet-derived growth wound healing. Below, data from animal models, patients factor, tumor necrosis factor, and interleukin-1a in wounded with Cushing syndrome, and clinical studies are reviewed. 412 The American Journal of Surgery, Vol 206, No 3, September 2013 Effect of corticosteroid dose on wound healing wound tensile strength, should be considered more clinically relevant outcome measures. A number of animal studies have quantified the effects of high-dose corticosteroids on wound tensile strength and Effect of chronicity of corticosteroid anastomotic bursting pressures (Table 1).14–27 Comparing administration on wound healing these animal studies as a group is
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