The skin microbiome of infected pressure ulcers: A review and implications for health professionals.
biofilms
coinfection
microbiota
pathogenic agents
pressure ulcer
skin diseases
Journal
European journal of clinical investigation
ISSN: 1365-2362
Titre abrégé: Eur J Clin Invest
Pays: England
ID NLM: 0245331
Informations de publication
Date de publication:
Jan 2022
Jan 2022
Historique:
revised:
27
09
2021
received:
26
07
2021
accepted:
29
09
2021
pubmed:
4
10
2021
medline:
18
3
2022
entrez:
3
10
2021
Statut:
ppublish
Résumé
Pressure ulcers (PUs) are injuries resulting from ischaemia caused by prolonged compression or shear forces on the skin, adjacent tissues and bones. Advanced stages of PUs are associated with infectious complications and constitute a major clinical challenge, with high social and economic impacts in health care. This study aims to identify and describe the relationship between PU risk factors, stages and anatomical locations, and the relevance of microbial cohabitation and biofilm growth. The narrative review method to advocating a critical and objective analysis of the current knowledge on the topic was performed. Indexed databases and direct consultation to specialized and high-impact journals on the subject were used to extract relevant information, guided by co-authors. The Medical Subject Headings of pressure ulcer (or injury), biofilms, infection and other analogues terms were used. Development of PUs and consequent infection depends on several direct and indirect risk factors, including cutaneous/PU microbiome, microclimate and behavioural factors. Infected PUs are polymicrobial and characterized by biofilm-associated infection, phenotypic hypervariability of species and inherent resistance to antimicrobials. The different stages and anatomical locations also play an important role in their colonization. The prevention and monitoring of PUs remain crucial for avoiding the emergence of systemic infections and reducing health care-associated costs, improve the quality of life of patients and reduce the mortality-associated infected PUs.
Sections du résumé
BACKGROUND
BACKGROUND
Pressure ulcers (PUs) are injuries resulting from ischaemia caused by prolonged compression or shear forces on the skin, adjacent tissues and bones. Advanced stages of PUs are associated with infectious complications and constitute a major clinical challenge, with high social and economic impacts in health care.
GOALS
OBJECTIVE
This study aims to identify and describe the relationship between PU risk factors, stages and anatomical locations, and the relevance of microbial cohabitation and biofilm growth.
METHODS
METHODS
The narrative review method to advocating a critical and objective analysis of the current knowledge on the topic was performed. Indexed databases and direct consultation to specialized and high-impact journals on the subject were used to extract relevant information, guided by co-authors. The Medical Subject Headings of pressure ulcer (or injury), biofilms, infection and other analogues terms were used.
RESULTS
RESULTS
Development of PUs and consequent infection depends on several direct and indirect risk factors, including cutaneous/PU microbiome, microclimate and behavioural factors. Infected PUs are polymicrobial and characterized by biofilm-associated infection, phenotypic hypervariability of species and inherent resistance to antimicrobials. The different stages and anatomical locations also play an important role in their colonization. The prevention and monitoring of PUs remain crucial for avoiding the emergence of systemic infections and reducing health care-associated costs, improve the quality of life of patients and reduce the mortality-associated infected PUs.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13688Subventions
Organisme : Operational Programme for Competitiveness and Internationalisation/ Partnership Agreement, through the European Regional Development Fund (ERDF)
ID : POCI-01-0247-FEDER-039869
Informations de copyright
© 2021 Stichting European Society for Clinical Investigation Journal Foundation. Published by John Wiley & Sons Ltd.
Références
Taradaj J. Prevention and treatment of pressure ulcers by newest recommendations from European pressure ulcer advisory panel (EPUAP): practical reference guide for GPs. Fam Med Prim Care Rev. 2017;19:81-83.
Edsberg LE, Black JM, Goldberg M, McNichol L, Moore L, Sieggreen M. Revised national pressure ulcer advisory panel pressure injury staging system. J Wound Ostomy Cont Nurs. 2016;43:585-597.
National Pressure Ulcer Advisory and Pan Pacific Pressure Injury Alliance. Prevention and treatment of pressure ulcers: quick reference guide. Clinical practice guideline. Osborne Park, Australia; 2014: National Pressure Ulcer Advisory and Pan Pacific Pressure Injury Alliance; 2015.
Theisen S, Drabik A, Stock S. Pressure ulcers in older hospitalised patients and its impact on length of stay: a retrospective observational study. J Clin Nurs. 2012;21:380-387.
Vanderwee K, Clark M, Dealey C, Gunningberg L, Defloor T. Pressure ulcer prevalence in Europe: a pilot study. J Eval Clin Pract. 2007;13:227-235.
Agrawal K, Chauhan N. Pressure ulcers: back to the basics. Indian J Plast Surg. 2012;45:244-254.
Woodbury MG. Prevalence of pressure; 2014.
González-Méndez MI, Lima-Serrano M, Martín-Castaño C, Alonso-Araujo I, Lima-Rodríguez JS. Incidence and risk factors associated with the development of pressure ulcers in an intensive care unit. J Clin Nurs. 2018;27:1028-1037.
Martinengo L, Olsson M, Bajpai R, et al. Prevalence of chronic wounds in the general population: systematic review and meta-analysis of observational studies. Ann Epidemiol. 2019;29:8-15.
Scheel-Sailer A, Wyss A, Boldt C, Post MW, Lay V. Prevalence, location, grade of pressure ulcers and association with specific patient characteristics in adult spinal cord injury patients during the hospital stay: a prospective cohort study. Spinal Cord. 2013;51:828-833.
Smith MEB, Totten A, Hickam DH, et al. Pressure ulcer treatment strategies: a systematic comparative effectiveness review. Ann Intern Med. 2013;159:39-50.
Whitty JA, McInnes E, Bucknall T, et al. The cost-effectiveness of a patient centred pressure ulcer prevention care bundle: findings from the INTACT cluster randomised trial. Int J Nurs Stud. 2017;75:35-42.
Mervis JS, Phillips TJ. Pressure ulcers: pathophysiology, epidemiology, risk factors, and presentation. J Am Acad Dermatol. 2019;81:881-890.
Medical Advisory Secretariat. Management of chronic pressure ulcers: an evidence-based analysis. Ont Health Technol Assess Ser. 2009;9(3): 1-203.
Negut I, Grumezescu V, Grumezescu AM. Treatment strategies for infected wounds. Molecules. 2018;23:1-23.
Stevens DL, Bryant AE. Impetigo, erysipelas and cellulitis. In: Ferretti JJ, Stevens DL, Fischetti VA, eds. Streptococcus pyogenes: Basic Biology to Clinical Manifestations; Oklahoma, USA: University of Oklahoma Health Sciences Center; 2016:1-18.
Livesley NJ, Chow AW. Infected pressure ulcers in elderly individuals. Clin Infect Dis. 2002;35:1390-1396.
Reilly E, Karakousis G, Schrag S, Stawicki S. Pressure ulcers in the intensive care unit: the ‘forgotten’ enemy. Opus. 2007;12:17-30.
Boyko TV, Longaker MT, Yang GP. Review of the current management of pressure ulcers. Adv Wound Care. 2018;7:57-67.
Bluestein D, Javaheri A. Pressure ulcers: prevention, evaluation, and management. Am Fam Physician. 2008;78:1186-1194.
Dana AN, Bauman WA. Bacteriology of pressure ulcers in individuals with spinal cord injury: what we know and what we should know. J Spinal Cord Med. 2015;38:147-160.
Biglari B, vd Linden PH, Simon A, et al. Use of Medihoney as a non-surgical therapy for chronic pressure ulcers in patients with spinal cord injury. Spinal Cord. 2012;50:165-169.
Wolcott RD, Hanson JD, Rees EJ, et al. Analysis of the chronic wound microbiota of 2,963 patients by 16S rDNA pyrosequencing. Wound Repair Regen. 2016;24:163-174.
Espejo E, Andrés M, Borrallo RM, Padilla E, Garcia-Restoy E, Bella F. Bacteremia associated with pressure ulcers: a prospective cohort study. Eur J Clin Microbiol Infect Dis. 2018;37:969-975.
Andrianasolo J, Ferry T, Boucher F, et al. Pressure ulcer-related pelvic osteomyelitis: evaluation of a two-stage surgical strategy (debridement, negative pressure therapy and flap coverage) with prolonged antimicrobial therapy. BMC Infect Dis. 2018;18:1-11.
de Wert LA, Rensen SS, Soons Z, Poeze M, Bouvy ND, Penders J. The cutaneous microbiome in hospitalized patients with pressure ulcers. Sci Rep. 2020;10:1-11.
Nagase S, Ogai K, Urai T, et al. Distinct skin microbiome and skin physiological functions between bedridden older patients and healthy people: a single-center study in Japan. Front Med. 2020;7:1-12.
Kunimitsu M, Nakagami G, Kitamura A, et al. The combination of high bacterial count and positive biofilm formation is associated with the inflammation of pressure ulcers. Chronic Wound Care Manag Res. 2019;6: 1-7.
Percival SL, McCarty SM, Lipsky B. Biofilms and wounds: an overview of the evidence. Adv Wound Care. 2015;4:373-381.
Findley K, Grice EA. The skin microbiome: a focus on pathogens and their association with skin disease. PLoS Pathog. 2014;10:10-12.
Byrd AL, Belkaid Y, Segre JA. The human skin microbiome. Nat Rev Microbiol. 2018;16:143-155.
Braga IA, Brito CS, Filho AD, Filho PPG, Ribas RM. Pressure ulcer as a reservoir of multiresistant Gram-negative bacilli: risk factors for colonization and development of bacteremia. Braz J Infect Dis. 2017;21:171-175.
Baethge C, Goldbeck-Wood S, Mertens S. SANRA-a scale for the quality assessment of narrative review articles. Res Integr Peer Rev. 2019;4:2-8.
Smith DM, Snow DE, Rees E, et al. Evaluation of the bacterial diversity of pressure ulcers using bTEFAP pyrosequencing. BMC Med Genomics. 2010;3:17-19.
Mehmood M, Jaffar NA, Nazim M, Khasawneh FA. Bacteremic skin and soft tissue infection caused by Prevotella loescheii. BMC Infect Dis. 2014;14:2-5.
Takamura N, Tada K, Ishioka H, Gomi H. Clinically infrequent arcanobacterium haemolyticum bacteremia complicated by foot decubitus ulcer: an educational reminder for primary care physicians. Intern Med. 2019;58:1645-1647.
Braga IA, Pirett CCNS, Ribas RM, Filho PPG, Filho AD. Bacterial colonization of pressure ulcers: assessment of risk for bloodstream infection and impact on patient outcomes. J Hosp Infect. 2013;83:314-320.
Ammons MCB, Morrissey K, Tripet BP, et al. Biochemical association of metabolic profile and microbiome in chronic pressure ulcer wounds. PLoS One. 2015;10:1-22.
Brauncajs M, Ksiąszczyk K, Lewandowska-Polak A, Gorzela K, Grzegorczyk J. Impact of low-level laser therapy on the dynamics of pressure ulcer-induced changes considering an infectious agent and cathelicidin LL-37 concentration: a preliminary study. Adv Dermatol Allergol. 2018;35:582-586.
Kučišec-Tepeš N. Characteristic features of pressure ulcer infection. Acta Med Croat. 2016;70:45-51.
Galivanche AR, Kebaish KJ, Adrados M, et al. Postoperative pressure ulcers after geriatric hip fracture surgery are predicted by defined preoperative comorbidities and postoperative complications. J Am Acad Orthop Surg. 2020;28:342-351.
Heinzelmann M, Scott M, Lam T. Factors predisposing to bacterial invasion and infection. Am J Surg. 2002;183:179-190.
Coleman S, Gorecki C, Nelson EA, et al. Patient risk factors for pressure ulcer development: systematic review. Int J Nurs Stud. 2013;50:974-1003.
Li J, Chen J, Kirsner R. Pathophysiology of acute wound healing. Clin Dermatol. 2007;25:9-18.
Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15:167-193.
Moura J, Madureira P, Leal EC, Fonseca AC, Carvalho E. Immune aging in diabetes and its implications in wound healing. Clin Immunol. 2019;200:43-54.
Ogai K, Ogura K, Ohgi N, et al. Stability of skin microbiome at sacral regions of healthy young adults, ambulatory older adults, and bedridden older patients after 2 years. Biol Res Nurs. 2021;23:82-90.
Shumer DE, N. J. N. N. P. S. 乳鼠心肌提取 HHS public access. Physiol Behav. 2017;176:139-148.
, Balaji U, Porembka MR, Wachsmann MB, et. al Immunologic and Metabolic Features of Pancreatic Ductal Adenocarcinoma Define Prognostic Subtypes of Disease. Clinical Cancer Research. 2016;22:(14):3606-3617. http://dx.doi.org/10.1158/1078-0432.ccr-15-1883
Bhattacharya S, Mishra R. Pressure ulcers: current understanding and newer modalities of treatment. Indian J Plast Surg. 2015;48:4-16.
Vandegrift R, Bateman AC, Siemens KN, et al. Cleanliness in context: reconciling hygiene with a modern microbial perspective. Microbiome. 2017;5:76.
Arnold M, Barbul A. Nutrition and wound healing. Plast Reconstr Surg. 2006;117:42-58.
Coates M, Mariottoni P, Corcoran DL, et al. The skin transcriptome in hidradenitis suppurativa uncovers an antimicrobial and sweat gland gene signature which has distinct overlap with wounded skin. PLoS One. 2019;14:1-24.
SanMiguel AJ, Meisel JS, Horwinski J, Zheng Q, Bradley CW, Grice EA. Body site-specific shifts in resident. Skin. 2019;138:2234-2243.
Kottner J, Black J, Call E, Gefen A, Santamaria N. Microclimate: a critical review in the context of pressure ulcer prevention. Clin Biomech. 2018;59:62-70.
Leyva-Mendivil MF, Lengiewicz J, Page A, Bressloff NW, Limbert G. Skin microstructure is a key contributor to its friction behaviour. Tribol Lett. 2017;65:1-17.
Yusuf S, Okuwa M, Shigeta Y, et al. Microclimate and development of pressure ulcers and superficial skin changes. Int Wound J. 2015;12:40-46.
International Review. Pressure, shear, friction and microclimate in context: a consensus document. Wounds International. 2010;1(1):1-28.
Gefen A. How do microclimate factors affect the risk for superficial pressure ulcers: a mathematical modeling study. J Tissue Viability. 2011;20:81-88.
Strohal R, Mittlböck M, Hämmerle G. The management of critically colonized and locally infected leg ulcers with an acid-oxidizing solution: a pilot study. Adv Skin Wound Care. 2018;31:163-171.
Song SJ, Lauber C, Costello EK, et al. Cohabiting family members share microbiota with one another and with their dogs. Elife. 2013;2013:1-22.
Ying S, Zeng D-N, Chi L, et al. The influence of age and gender on skin-associated microbial communities in urban and rural human populations. PLoS One. 2015;10:1-16.
Stojadinovic O, Minkiewicz J, Sawaya A, et al. Deep tissue injury in development of pressure ulcers: a decrease of inflammasome activation and changes in human skin morphology in response to aging and mechanical load. PLoS One. 2013;8:1-9.
Lumbers M. Cause, risk and management. Br J Nurs. 2018;27:6-14.
Zheng D, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020;30:(6)492-506. https://doi.org/10.1038/s41422-020-0332-7
Sibbald RG, Mufti A, Armstrong D. Infrared skin thermometry: an underutilized cost-effective tool for routine wound care. Adv Skin Wound Care. 2015;28:37-44.
Miller MA, Zachary JF. Mechanisms and morphology of cellular injury, adaptation, and death. Pathol Basis Vet Dis. e19. 1. University of Illinois, Urbana, Illinois - USA: Elsivier Public Health Emergency; 2017:2-43.
Jaul E, Barron J, Rosenzweig JP, Menczel J. An overview of co-morbidities and the development of pressure ulcers among older adults. BMC Geriatr. 2018;18:1-11.
Stechmiller JK. Understanding the role of nutrition and wound healing. Nutr Clin Pract. 2010;25:61-68.
Cereda E, Klersy C, Serioli M, Crespi A, D'Andrea F. A nutritional formula enriched with arginine, zinc, and antioxidants for the healing of pressure ulcers: a randomized trial. Ann Intern Med. 2015;162:167-174.
Guo S, DiPietro LA. Critical review in oral biology & medicine: factors affecting wound healing. J Dent Res. 2010;89:219-229.
Hugonnet S, Chevrolet JC, Pittet D. The effect of workload on infection risk in critically ill patients. Crit Care Med. 2007;35:76-81.
Zimlichman E, Henderson D, Tamir O, et al. Health care-associated infections: a meta-analysis of costs and financial impact on the US health care system. JAMA Intern Med. 2013;173:2039-2046.
Donelli G. Biofilm-based healthcare-associated infections: volume II. Adv Exp Med Biol. 2015;831:11-27.
Espinosa A, Palencia S, Garcia A, Palencia M. Polymicrobial biofilms: fundamentals, diseases, and treatments - a review. J Sci Technol Appl. 2020;8:4-34.
Haque M, Sartelli M, Mckimm J, Abu Bakar M. Infection and drug resistance dovepress health care-associated infections - an overview. Infect Drug Resist. 2018;11:2321-2333.
Dowd SE, Delton Hanson J, Rees E, et al. Survey of fungi and yeast in polymicrobial infections in chronic wounds. J Wound Care. 2011;20:40-47.
Foroozan M, Contet Audonneau N, Granel-Brocard F, Barbaud A, Schmutz J. Prevalence analysis of fungi in chronic lower extremity ulcers. Wounds. 2011;23(3):68-75.
Brem H, Lyder C. Protocol for the successful treatment of pressure ulcers. Am J Surg. 2004;188:9-17.
Llor C, Bjerrum L. Antimicrobial resistance: risk associated with antibiotic overuse and initiatives to reduce the problem. Ther Adv Drug Saf. 2014;5:229-241.
Nakagami G, Schultz G, Kitamura A, et al. Rapid detection of biofilm by wound blotting following sharp debridement of chronic pressure ulcers predicts wound healing: a preliminary study. Int Wound J. 2020;17:191-196.
Donelli G, Vuotto C. Biofilm-based infections in long-term care facilities. Future Microbiol. 2014;9:175-188.
James GA, Swogger E, Wolcott R, et al. Biofilms in chronic wounds. Wound Repair Regen. 2008;16:37-44.
Wei DI, Zhu X-M, Chen Y-Y, et al. Chronic wound biofilms: diagnosis and therapeutic strategies. Chin Med J. 2019;132:2737-2744.
Nadell CD, Drescher K, Wingreen NS, Bassler BL. Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME J. 2015;9:1700-1709.
Percival SL, Suleman L, Vuotto C, Donelli G. Healthcare-associated infections, medical devices and biofilms: risk, tolerance and control. J Med Microbiol. 2015;64(4):323-334. doi:10.1099/jmm.0.000032
Zhao X, Yu Z, Ding T. Quorum-sensing regulation of antimicrobial resistance in bacteria. Microorganisms. 2020;8:1-21.
Jensen PØ, Kolpen M, Kragh KN, Kühl M. Microenvironmental characteristics and physiology of biofilms in chronic infections of CF patients are strongly affected by the host immune response. APMIS. 2017;125:276-288.
Vasudevan R. Biofilms: microbial cities of scientific significance. J Microbiol Exp. 2014;1:00014.
Bjarnsholt T. The role of bacterial biofilms in chronic infections. APMIS. 2013;121:1-58.
Hatabe Y, Shibata M, Ohara T, et al. Decline in handgrip strength from midlife to late-life is associated with dementia in a Japanese community: the Hisayama study. J Epidemiol. 2020;30:15-23.
Malone M, Bjarnsholt T, McBain AJ, et al. The prevalence of biofilms in chronic wounds: a systematic review and meta-analysis of published data. J. Wound Care. 2017;26.
Wolcott R, Dowd S. The role of biofilms: are we hitting the right target? Plast Reconstr Surg. 2011;127:28S-35S.
Bowler PG, Duerden BI, Armstrong DG. Wound microbiology and associated approaches to wound management. Clin Microbiol Rev. 2001;14:244-269.
Porreca EG, Giordano-Jablon GM. Treatment of severe (Stage III and IV) chronic pressure ulcers using pulsed radio frequency energy in a quadriplegic patient. Eplasty. 2008;8:e49.
Chaves ME, Silva FS, Soares VP, et al. Evaluation of healing of pressure ulcers through thermography: a preliminary study. Rev Bras Eng Biomed. 2015;31:3-9.
Russell CD, Tsang ST, Sutherland RK. Outcomes, microbiology and antimicrobial usage in pressure ulcer-related pelvic osteomyelitis: messages for clinical practice. J Bone Jt Infect. 2020;5:67-75.
Diaz-Caro I, Garcia Gomez-Heras S. Incidence of hospital-acquired pressure ulcers in patients with ‘minimal risk’ according to the ‘norton-MI’ scale. PLoS One. 2020;15:1-16.
Sato M, Sanada H, Konya C, Sugama J, Nakagami G. Prognosis of stage I pressure ulcers and related factors. Int Wound J. 2006;3:355-362.
Bennett G, Dealey C, Posnett J. The cost of pressure ulcers in the UK. Age Ageing. 2004;33:230-235.
Palese A, Saiani L, Pota I, et al. What is the healing time of stage II pressure ulcers? Findings from a secondary analysis. Adv Skin Wound Care. 2015;28:69-75.
Sullivan T, De Barra E. Diagnosis and management of cellulitis. Clin Med J R Coll Physicians London. 2018;18:160-163.
Brunel A-S, Lamy B, Cyteval C, et al. Diagnosing pelvic osteomyelitis beneath pressure ulcers in spinal cord injured patients: a prospective study. Clin Microbiol Infect. 2016;22(3):267.e1-8.
Garcia AD, Thomas DR. Assessment and management of chronic pressure ulcers in the elderly. Med Clin North Am. 2006;90:925-944.
Dolati M, Honarmand JS, Javadi A, Zare Kariz S, Ghobadi SB. Phenotypic and molecular identification of bacteria involved in decubitus ulcers. J Med Bacteriol. 2017;6:45-55.
Sadeghi Fazel F, Mohammadnejad A, Amanpour S, et al. Bacteriology and antimicrobial sensitivity of isolated bacteria from pressure ulcers after spinal cord injury. Arch Neurosci. 2019 in press.