{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,12]],"date-time":"2026-10-12T22:22:55Z","timestamp":1791843775295,"version":"4.3.4"},"reference-count":40,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,5,1]],"date-time":"2021-05-01T00:00:00Z","timestamp":1619827200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Multidrug-resistant organism infections have become important in recent years due to the increased prevalence of diabetic foot ulcers and their possible consequences. This study aimed to systematically review and evaluate ulcer duration, healing time, hospital stay, amputation, and mortality rates in patients with diabetic foot ulcers caused by infection with multidrug-resistant organisms. PubMed, the Cochrane Library, and Web of Science were searched in May 2020 to find observational studies in English about the clinical outcomes of multidrug-resistant organism infection in diabetic foot ulcers. Eight studies met the inclusion criteria, and these studies included 923 patients. The overall methodological quality of the study was moderate. Ulcer duration was described in six studies, and there was no practical association with multidrug-resistant organisms. Two out of three studies reported a longer healing time in multidrug-resistant organism infections than in non-multidrug-resistant organism infections. Clinical outcomes included the duration of hospitalisation, surgeries, amputations, and deaths. Lower limb amputation was the most reported clinical outcome in the included studies, and was more prevalent in the multidrug-resistant organism infections. We concluded that there was not enough evidence that multidrug-resistant organisms hindered the healing of diabetic foot ulcers. In contrast to the clinical outcomes, multidrug-resistant organisms affect both amputation rates and mortality rates.<\/jats:p>","DOI":"10.3390\/jcm10091948","type":"journal-article","created":{"date-parts":[[2021,5,1]],"date-time":"2021-05-01T21:35:39Z","timestamp":1619904939000},"page":"1948","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":52,"title":["The Influence of Multidrug-Resistant Bacteria on Clinical Outcomes of Diabetic Foot Ulcers: A Systematic Review"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2578-5938","authenticated-orcid":false,"given":"Gianmarco","family":"Matta-Guti\u00e9rrez","sequence":"first","affiliation":[{"name":"Diabetic Foot Unit, Cl\u00ednica Universitaria de Podolog\u00eda, Facultad de Enfermer\u00eda, Fisioterapia y Podolog\u00eda, Universidad Complutense de Madrid, Instituto de Investigaci\u00f3n Sanitaria del Hospital Cl\u00ednico San Carlos (IdISSC), 28040 Madrid, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3896-7079","authenticated-orcid":false,"given":"Esther","family":"Garc\u00eda-Morales","sequence":"additional","affiliation":[{"name":"Diabetic Foot Unit, Cl\u00ednica Universitaria de Podolog\u00eda, Facultad de Enfermer\u00eda, Fisioterapia y Podolog\u00eda, Universidad Complutense de Madrid, Instituto de Investigaci\u00f3n Sanitaria del Hospital Cl\u00ednico San Carlos (IdISSC), 28040 Madrid, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1424-5087","authenticated-orcid":false,"given":"Yolanda","family":"Garc\u00eda-\u00c1lvarez","sequence":"additional","affiliation":[{"name":"Diabetic Foot Unit, Cl\u00ednica Universitaria de Podolog\u00eda, Facultad de Enfermer\u00eda, Fisioterapia y Podolog\u00eda, Universidad Complutense de Madrid, Instituto de Investigaci\u00f3n Sanitaria del Hospital Cl\u00ednico San Carlos (IdISSC), 28040 Madrid, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4674-3822","authenticated-orcid":false,"given":"Francisco Javier","family":"\u00c1lvaro-Afonso","sequence":"additional","affiliation":[{"name":"Diabetic Foot Unit, Cl\u00ednica Universitaria de Podolog\u00eda, Facultad de Enfermer\u00eda, Fisioterapia y Podolog\u00eda, Universidad Complutense de Madrid, Instituto de Investigaci\u00f3n Sanitaria del Hospital Cl\u00ednico San Carlos (IdISSC), 28040 Madrid, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ra\u00fal Juan","family":"Molines-Barroso","sequence":"additional","affiliation":[{"name":"Diabetic Foot Unit, Cl\u00ednica Universitaria de Podolog\u00eda, Facultad de Enfermer\u00eda, Fisioterapia y Podolog\u00eda, Universidad Complutense de Madrid, Instituto de Investigaci\u00f3n Sanitaria del Hospital Cl\u00ednico San Carlos (IdISSC), 28040 Madrid, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6110-0265","authenticated-orcid":false,"given":"Jos\u00e9 Luis","family":"L\u00e1zaro-Mart\u00ednez","sequence":"additional","affiliation":[{"name":"Diabetic Foot Unit, Cl\u00ednica Universitaria de Podolog\u00eda, Facultad de Enfermer\u00eda, Fisioterapia y Podolog\u00eda, Universidad Complutense de Madrid, Instituto de Investigaci\u00f3n Sanitaria del Hospital Cl\u00ednico San Carlos (IdISSC), 28040 Madrid, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,5,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1288","DOI":"10.2337\/dc05-2425","article-title":"Risk Factors for Foot Infections in Individuals With Diabetes","volume":"29","author":"Lavery","year":"2006","journal-title":"Diabetes Care"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1186\/s13047-020-00383-2","article-title":"Five year mortality and direct costs of care for people with diabetic foot complications are comparable to cancer","volume":"13","author":"Armstrong","year":"2020","journal-title":"J. Foot Ankle Res."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"528","DOI":"10.1086\/590012","article-title":"Bone of Contention: Diagnosing Diabetic Foot Osteomyelitis","volume":"47","author":"Lipsky","year":"2008","journal-title":"Clin. Infect. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1080","DOI":"10.1021\/acs.accounts.0c00864","article-title":"Strategy for Treatment of Infected Diabetic Foot Ulcers","volume":"54","author":"Chang","year":"2021","journal-title":"Acc. Chem. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"S123","DOI":"10.1086\/383273","article-title":"Surgical Treatment of the Infected Diabetic Foot","volume":"39","year":"2004","journal-title":"Clin. Infect. Dis."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1002\/dmrr.2699","article-title":"Arag\u00f3n-S\u00e1nchez J, Diggle M, Embil J, Kono S, Lavery L; et al. IWGDF guidance on the diagnosis and management of foot infections in persons with diabetes","volume":"32","author":"Lipsky","year":"2016","journal-title":"Diabetes Metab. Res. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e3280","DOI":"10.1002\/dmrr.3280","article-title":"Guidelines on the diagnosis and treatment of foot infection in persons with diabetes (IWGDF 2019 update)","volume":"36","author":"Lipsky","year":"2020","journal-title":"Diabetes Metab. Res. Rev."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e132","DOI":"10.1093\/cid\/cis346","article-title":"2012 Infectious Diseases Society of America Clinical Practice Guideline for the Diagnosis and Treatment of Diabetic","volume":"54","author":"Lipsky","year":"2012","journal-title":"Foot Infect. Clin. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1080\/14787210.2018.1417037","article-title":"Modern management of diabetic foot osteomyelitis. The when, how and why of conservative approaches","volume":"16","author":"Lipsky","year":"2018","journal-title":"Expert Rev. Anti Infect. Ther."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"11","DOI":"10.3947\/ic.2018.50.1.11","article-title":"Microbiology and Antimicrobial Therapy for Diabetic Foot Infections","volume":"50","author":"Kwon","year":"2018","journal-title":"Infect. Chemother"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1785","DOI":"10.2165\/11538070-000000000-00000","article-title":"Methicillin-Resistant Staphylococcus aureus in Diabetic Foot Infections","volume":"70","author":"Eleftheriadou","year":"2010","journal-title":"Drugs"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1007\/s00592-019-01301-0","article-title":"The prevalence of methicillin-resistant Staphylococcus aureus among diabetic patients: A meta-analysis","volume":"56","author":"Stacey","year":"2019","journal-title":"Acta Diabetol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.ijid.2018.02.013","article-title":"Influence of multidrug resistant organisms on the outcome of diabetic foot infection","volume":"70","author":"Saltoglu","year":"2018","journal-title":"Int. J. Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1177\/1534734617728642","article-title":"The Relationship Between Osteomyelitis Complication and Drug-Resistant Infection Risk in Diabetic Foot Ulcer: A Meta-analysis","volume":"16","author":"Chen","year":"2017","journal-title":"Int. J. Low. Extrem. Wounds"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1177\/1534734614521236","article-title":"Clinical Characteristics and Risk Factors of Diabetic Foot Ulcer With Multidrug-Resistant Organism Infection","volume":"13","author":"Ji","year":"2014","journal-title":"Int. J. Low. Extrem. Wounds"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Dai, J., Jiang, C., Chen, H., and Chai, Y. (2019). Assessment of the Risk Factors of Multidrug-Resistant Organism Infection in Adults With Type 1 or Type 2 Diabetes and Diabetic Foot Ulcer. Can. J. Diabetes, 1\u20138.","DOI":"10.1016\/j.jcjd.2019.10.009"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1111\/j.1464-5491.2004.01237.x","article-title":"Diabetic foot ulcer and multidrug-resistant organisms: Risk factors and impact","volume":"21","author":"Robert","year":"2004","journal-title":"Diabet. Med."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1727","DOI":"10.2337\/dc06-0116","article-title":"A Clinico-microbiological Study of Diabetic Foot Ulcers in an Indian Tertiary Care Hospital","volume":"29","author":"Gadepalli","year":"2006","journal-title":"Diabetes Care"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/j.jinf.2006.08.013","article-title":"Risk factors for infection of the diabetic foot with multi-antibiotic resistant microorganisms","volume":"54","author":"Kandemir","year":"2007","journal-title":"J. Infect."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1177\/1534734614545878","article-title":"Clinical Outcomes of Multidrug Resistant Pseudomonas aeruginosa Infection and the Relationship With Type III Secretion System in Patients With Diabetic Foot","volume":"13","author":"Zhang","year":"2014","journal-title":"Int. J. Low. Extrem. Wounds"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.foot.2017.05.001","article-title":"Inflammatory markers as risk factors for infection with multidrug-resistant microbes in diabetic foot subjects","volume":"32","author":"Noor","year":"2017","journal-title":"Foot"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.foot.2010.10.003","article-title":"Clinico-microbiological study and antimicrobial drug resistance profile of diabetic foot infections in North India","volume":"21","author":"Zubair","year":"2010","journal-title":"Foot"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1016\/j.diabet.2008.02.005","article-title":"Risk factors and healing impact of multidrug-resistant bacteria in diabetic foot ulcers","volume":"34","author":"Richard","year":"2008","journal-title":"Diabetes Metab."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"264","DOI":"10.7326\/0003-4819-151-4-200908180-00135","article-title":"Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement","volume":"151","author":"Moher","year":"2009","journal-title":"Ann. Intern. Med."},{"key":"ref_25","unstructured":"Oxford Centre for Evidence-Based Medicine (2020, May 30). Levels of Evidence (March 2009) 2009. Available online: http:\/\/www.cebm.net\/oxford-centre-evidence-based-medicine-levels-evidence-march-2009\/."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1016\/S0140-6736(07)61602-X","article-title":"The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for reporting observational studies","volume":"370","author":"Altman","year":"2007","journal-title":"Lancet"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1016\/S0030-5898(20)31101-9","article-title":"Bacterial adherence and the glycocalyx and their role in musculoskeletal infection","volume":"15","author":"Gristina","year":"1984","journal-title":"Orthop. Clin. N. Am."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1111\/dom.12190","article-title":"Diabetic foot infections: State-of-the-art. Diabetes","volume":"16","author":"Gariani","year":"2014","journal-title":"Obes. Metab."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1016\/j.bjm.2017.09.003","article-title":"Epidemiology of diabetic foot infections in a reference tertiary hospital in India","volume":"49","author":"Saseedharan","year":"2018","journal-title":"Braz. J. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1177\/1534734619866610","article-title":"Clinical and Antimicrobial Efficacy of a Silver Foam Dressing With Silicone Adhesive in Diabetic Foot Ulcers With Mild Infection","volume":"18","year":"2019","journal-title":"Int. J. Low. Extrem. Wounds"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"855","DOI":"10.2337\/diacare.21.5.855","article-title":"Validation of a Diabetic Wound Classification System: The contribution of depth, infection, and ischemia to risk of amputation","volume":"21","author":"Armstrong","year":"1998","journal-title":"Diabetes Care"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1086\/511036","article-title":"Validation of the Infectious Diseases Society of America\u2019s Diabetic Foot Infection Classification System","volume":"44","author":"Lavery","year":"2007","journal-title":"Clin. Infect. Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1080\/02713680500536746","article-title":"Type III Secretion System\u2013Associated Toxins, Proteases, Serotypes, and Antibiotic Resistance of Pseudomonas aeruginosa Isolates Associated with Keratitis","volume":"31","author":"Zhu","year":"2006","journal-title":"Curr. Eye Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1695","DOI":"10.1086\/379372","article-title":"Secretion of the Toxin ExoU Is a Marker for Highly Virulent Pseudomonas aeruginosa Isolates Obtained from Patients with Hospital-Acquired Pneumonia","volume":"188","author":"Schulert","year":"2003","journal-title":"J. Infect. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"3706","DOI":"10.2337\/dc13-1083","article-title":"SIRS Is Valid in Discriminating Between Severe and Moderate Diabetic Foot Infections","volume":"36","author":"Wukich","year":"2013","journal-title":"Diabetes Care"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1177\/1071100712467980","article-title":"Severity of Diabetic Foot Infection and Rate of Limb Salvage","volume":"34","author":"Wukich","year":"2013","journal-title":"Foot Ankle Int."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1086\/501641","article-title":"Nosocomial Methicillin-Resistant and Methicillin-Susceptible Staphylococcus Aureus Primary Bacteremia: At What Costs?","volume":"20","author":"Abramson","year":"1999","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1545","DOI":"10.1164\/ajrccm.150.6.7952612","article-title":"Ventilator-associated pneumonia by Staphylococcus aureus. Comparison of methicillin-resistant and methicillin-sensitive episodes","volume":"150","author":"Rello","year":"1994","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1086\/313650","article-title":"Pathogenic Significance of Methicillin Resistance for Patients with Staphylococcus aureus Bacteremia","volume":"30","author":"Soriano","year":"2000","journal-title":"Clin. Infect. Dis."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/10\/9\/1948\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:56:26Z","timestamp":1760162186000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/10\/9\/1948"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,1]]},"references-count":40,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,5]]}},"alternative-id":["jcm10091948"],"URL":"https:\/\/doi.org\/10.3390\/jcm10091948","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,1]]}}}