234
Views
0
CrossRef citations to date
0
Altmetric
REVIEW

The Global Prevalence of Methicillin-Resistant Staphylococcus Aureus in Patients with Diabetic Foot Ulcers: A Systematic Review and Meta-Analysis

, , , , &
Pages 563-574 | Received 31 Oct 2023, Accepted 16 Jan 2024, Published online: 03 Feb 2024

References

  • Kharroubi AT, Darwish HM. Diabetes mellitus: the epidemic of the century. World J Diabetes. 2015;6:850–867. doi:10.4239/wjd.v6.i6.850
  • Armstrong DG, Boulton AJM, Bus SA. Diabetic foot ulcers and their recurrence. N Engl J Med. 2017;376:2367–2375. doi:10.1056/NEJMra1615439
  • Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcers in patients with diabetes. JAMA. 2005;293:217–228. doi:10.1001/jama.293.2.217
  • Lipsky BA, Senneville É, Abbas ZG, et al. Guidelines on the diagnosis and treatment of foot infection in persons with diabetes (IWGDF 2019 update). Diabetes Metab Res. 2020;36(Suppl 1):e3280. doi:10.1002/dmrr.3280
  • Ndosi M, Wright-Hughes A, Brown S, et al. Prognosis of the infected diabetic foot ulcer: a 12-month prospective observational study. Diabet Med. 2018;35:78–88. doi:10.1111/dme.13537
  • Eleftheriadou I, Tentolouris N, Argiana V, et al. Methicillin-resistant Staphylococcus aureus in diabetic foot infections. Drugs. 2010;70(14):1785–1797. doi:10.2165/11538070-000000000-00000
  • Kerr M, Barron E, Chadwick P, et al. The cost of diabetic foot ulcers and amputations to the national health service in England. Diabet Med. 2019;36(8):995–1002. doi:10.1111/dme.13973
  • Macdonald KE, Boeckh S, Stacey HJ, et al. The microbiology of diabetic foot infections: a meta-analysis. BMC Infect Dis. 2021;21(1):770. doi:10.1186/s12879-021-06516-7
  • Moore J, Gooday C, Soliman R, et al. Reduction in the prevalence of methicillin-resistant Staphylococcus aureus in tissue and wound swab samples taken from outpatients attending a specialist diabetic foot clinic 2005–2021. Diabet Med. 2023;40(10):e15081. doi:10.1111/dme.15081
  • Tentolouris N, Jude EB, Smirnof I, et al. Methicillin-resistant Staphylococcus aureus: an increasing problem in a diabetic foot clinic. Diabet Med. 1999;16(9):767–771. doi:10.1046/j.1464-5491.1999.00132.x
  • Cosgrove SE, Sakoulas G, Perencevich EN, et al. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus Bacteremia: a meta-analysis. Clin Infect Dis. 2003;36(1):53–59. doi:10.1086/345476
  • Filice GA, Nyman JA, Lexau C, et al. Excess costs and utilization associated with methicillin resistance for patients with Staphylococcus aureus infection. Infect Control Hosp Epidemiol. 2010;31(4):365–373. doi:10.1086/651094
  • Hidron AI, Kourbatova EV, Halvosa JS, et al. Risk factors for colonization with Methicillin-Resistant Staphylococcus aureus (MRSA) in patients admitted to an urban hospital: emergence of community-associated MRSA nasal carriage. Clin Infect Dis. 2005;41(2):159–166. doi:10.1086/430910
  • Moher D, Shamseer L, Clarke M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4:1. doi:10.1186/2046-4053-4-1
  • Munn Z, Moola S, Riitano D, et al. The development of a critical appraisal tool for use in systematic reviews addressing questions of prevalence. Int J Health Policy Manag. 2014;3(3):123–128. doi:10.15171/ijhpm.2014.71
  • Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–560. doi:10.1136/bmj.327.7414.557
  • Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–1558. doi:10.1002/sim.1186
  • Hunter JP, Saratzis A, Sutton AJ, et al. In meta-analyses of proportion studies, funnel plots were found to be an inaccurate method of assessing publication bias. J Clin Epidemiol. 2014;67:897–903. doi:10.1016/j.jclinepi.2014.03.003
  • Ahmed TE. Bacteriology of diabetic foot infections. Saudi Med J. 2000;21:344–347.
  • Dang CN, Prasad YD, Boulton AJ, et al. Methicillin-resistant Staphylococcus aureus in the diabetic foot clinic: a worsening problem. Diabet Med. 2003;20(2):159–161. doi:10.1046/j.1464-5491.2003.00860.x
  • Shankar EM, Mohan V, Premalatha G, et al. Bacterial etiology of diabetic foot infections in South India. Eur J Intern Med. 2005;16(8):567–570. doi:10.1016/j.ejim.2005.06.016
  • Lipsky BA, Armstrong DG, Citron DM, et al. Ertapenem versus piperacillin/tazobactam for diabetic foot infections (SIDESTEP): prospective, randomised, controlled, double-blinded, multicentre trial. Lancet. 2005;366(9498):1695–1703. doi:10.1016/S0140-6736(05)67694-5
  • Tentolouris N, Petrikkos G, Vallianou N, et al. Prevalence of methicillin-resistant Staphylococcus aureus in infected and uninfected diabetic foot ulcers. Clin Microbiol Infect. 2006;12(2):186–189. doi:10.1111/j.1469-0691.2005.01279.x
  • Martínez-Gómez Dde A, Ramírez-Almagro C, Campillo-Soto A, et al. Infecciones del pie diabético. Prevalencia de los distintos microorganismos y sensibilidad a los antimicrobianos [Diabetic foot infections. Prevalence and antibiotic sensitivity of the causative microorganisms]. Enferm Infecc Microbiol Clin. 2009;27:317–321. Spanish. doi:10.1016/j.eimc.2008.07.004
  • Lagacé-Wiens PR, Ormiston D, Nicolle LE, et al. The diabetic foot clinic: not a significant source for acquisition of methicillin-resistant Staphylococcus aureus. Am J Infect Control. 2009;37:587–589. doi:10.1016/j.ajic.2008.11.006
  • Mendes JJ, Marques-Costa A, Vilela C, et al. Clinical and bacteriological survey of diabetic foot infections in Lisbon. Diabet Res Clin Pract. 2012;95:153–161. doi:10.1016/j.diabres.2011.10.001
  • Lipsky BA, Itani KM, Weigelt JA, et al. The role of diabetes mellitus in the treatment of skin and skin structure infections caused by methicillin-resistant Staphylococcus aureus: results from three randomized controlled trials. Int J Infect Dis. 2011;15:e140–e146. doi:10.1016/j.ijid.2010.10.003
  • Feng SH, Chu YJ, Wang PH, et al. Risk factors and gene type for infections of MRSA in diabetic foot patients in Tianjin, China. Int J Low Extrem Wounds. 2013;12:106–112. doi:10.1177/1534734613489991
  • Djahmi N, Messad N, Nedjai S, et al. Molecular epidemiology of Staphylococcus aureus strains isolated from inpatients with infected diabetic foot ulcers in an Algerian University Hospital. Clin Microbiol Infect. 2013;19:E398–E404. doi:10.1111/1469-0691.12199
  • Sugandhi P, Prasanth DA. Microbiological profile of bacterial pathogens from diabetic foot infections in tertiary care hospitals, Salem. Diabetes Metab Syndr. 2014;8:129–132. doi:10.1016/j.dsx.2014.07.004
  • Senneville E, Brière M, Neut C, et al. First report of the predominance of clonal complex 398 Staphylococcus aureus strains in osteomyelitis complicating diabetic foot ulcers: a national French study. Clin Microbiol Infect. 2014;20:O274–O277. doi:10.1111/1469-0691.12375
  • Małecki R, Rosiński K, Adamiec R. Etiological factors of infections in diabetic foot syndrome - attempt to define optimal empirical therapy. Adv Clin Exp Med. 2014;23:39–48. doi:10.17219/acem/37020
  • Lavery LA, Fontaine JL, Bhavan K, et al. Risk factors for methicillin-resistant Staphylococcus aureus in diabetic foot infections. Diabet Foot Ankle. 2014;5. doi:10.3402/dfa.v5.23575
  • Ahmed EF, Gad GF, Abdalla AM, et al. Prevalence of methicillin resistant Staphylococcus aureus among Egyptian patients after surgical interventions. Surg Infect. 2014;15:404–411. doi:10.1089/sur.2013.212
  • Perim MC, Borges JC, Celeste SR, et al. Aerobic bacterial profile and antibiotic resistance in patients with diabetic foot infections. Rev Soc Bras Med Tro. 2015;48:546–554. doi:10.1590/0037-8682-0146-2015
  • Parsa H, Samani S. Microbiological features and risk factors in patients with diabetic foot ulcers. Wounds. 2015;27:308–312.
  • Commons RJ, Robinson CH, Gawler D, et al. High burden of diabetic foot infections in the top end of Australia: an emerging health crisis (DEFINE study). Diabet Res Clin Pract. 2015;110(2):147–157. doi:10.1016/j.diabres.2015.09.016
  • Reveles KR, Duhon BM, Moore RJ, et al. Epidemiology of methicillin-resistant Staphylococcus aureus diabetic foot infections in a large academic hospital: implications for antimicrobial stewardship. PLoS One. 2016;11(8):e0161658. doi:10.1371/journal.pone.0161658
  • Pobiega M, Myjak I, Pomorska-Wesolowska M, et al. Virulence potential of Staphylococcus aureus strains isolated from diabetic foot ulcers among patients from Southern Poland. Curr Vasc Pharmacol. 2016;14(6):547–551. doi:10.2174/1570161114666160625083742
  • Wu WX, Liu D, Wang YW, et al. Empirical antibiotic treatment in diabetic foot infection: a study focusing on the culture and antibiotic sensitivity in a population from Southern China. Int J Low Extrem Wounds. 2017;16:173–182. doi:10.1177/1534734617725410
  • Dunyach-Remy C, Courtais-Coulon C, DeMattei C, et al. Link between nasal carriage of Staphylococcus aureus and infected diabetic foot ulcers. Diabetes Metab. 2017;43(2):167–171. doi:10.1016/j.diabet.2016.09.003
  • van Asten SAV, Mithani M, Peters EJG, et al. Complications during the treatment of diabetic foot osteomyelitis. Diabet Res Clin Pract. 2018;135:58–64. doi:10.1016/j.diabres.2017.06.002
  • Obeid M, Moughames E, Aboulhosn P, et al. Epidemiology and susceptibility profiles of diabetic foot infections in five hospitals in Lebanon. J Infect Dev Ctries. 2018;12(05):347–351. doi:10.3855/jidc.10063
  • Neves JM, Duarte B, Pinto M, et al. Diabetic foot infection: causative pathogens and empiric antibiotherapy considerations-the experience of a tertiary center. Int J Low Extrem Wounds. 2019;18(2):122–128. doi:10.1177/1534734619839815
  • Kananizadeh P, Ohadian Moghadam S, Sadeghi Y, et al. Molecular characteristics of Methicillin-Resistant Staphylococcus aureus (MRSA) isolated from diabetic foot infection. Iran J Pathol. 2019;14:329–337. doi:10.30699/ijp.2019.101092.2035
  • Ullah I, Ali SS, Ahmed I, et al. Bacteriological profile and antibiotic susceptibility patterns in diabetic foot infections, at lady reading hospital, Peshawar. J Ayub Med Coll Abbottabad. 2020;32(3):382–388.
  • Lin SY, Lin NY, Huang YY, et al. Methicillin-resistant Staphylococcus aureus nasal carriage and infection among patients with diabetic foot ulcer. J Microbiol Immunol Infect. 2020;53:292–299. doi:10.1016/j.jmii.2018.03.005
  • Kim JJ, Lydecker A, Davé R, et al. Diabetic foot infections: local prevalence of and case-control study of risk factors for methicillin-resistant Staphylococcus aureus and Pseudomonas aeruginosa. Open Forum Infect Dis. 2020;7:ofaa412. doi:10.1093/ofid/ofaa412
  • Jouhar L, Jaafar RF, Nasreddine R, et al. Microbiological profile and antimicrobial resistance among diabetic foot infections in Lebanon. Int Wound J. 2020;17:1764–1773. doi:10.1111/iwj.13465
  • Anafo RB, Atiase Y, Dayie NTKD, et al. Methicillin-Resistant Staphylococcus aureus (MRSA) infection of diabetic foot ulcers at a tertiary care hospital in Accra, Ghana. Pathogens. 2021;10(8):937. doi:10.3390/pathogens10080937
  • Woldeteklie AA, Kebede HB, Abdela AA, et al. Prevalence of extended-spectrum β-lactamase and carbapenemase producers of gram-negative bacteria, and methicillin-resistant Staphylococcus aureus in isolates from diabetic foot ulcer patients in Ethiopia. Infect Drug Resist. 2022;15:4435–4441. doi:10.2147/IDR.S371431
  • Stańkowska M, Garbacz K, Korzon-Burakowska A, et al. Microbiological, clinical and radiological aspects of diabetic foot ulcers infected with methicillin-resistant and -sensitive Staphylococcus aureus. Pathogens. 2022;11:701. doi:10.3390/pathogens11060701
  • Pany S, Sharma BM, Sen SK, et al. Association of PVL gene in MSSA and MRSA strains among diabetic ulcer patients from Odisha, India. Int J Low Extrem Wounds. 2022:15347346221091355. doi:10.1177/15347346221091355
  • Hockney SM, Steker D, Bhasin A, et al. Role of bone biopsy and deep tissue culture for antibiotic stewardship in diabetic foot osteomyelitis. J Antimicrob Chemother. 2022;77(12):3482–3486. doi:10.1093/jac/dkac345
  • Brondo J, Morneau K, Hopkins T, et al. Correlation between patients with Methicillin-Resistant Staphylococcus aureus (MRSA) nares colonization and MRSA diabetic foot infections. Int J Low Extrem Wounds. 2022;21:502–505. doi:10.1177/1534734620963570
  • Arfaoui A, Sallem RB, Fernández-Fernández R, et al. Methicillin-resistant Staphylococcus aureus from diabetic foot infections in a Tunisian hospital with the first detection of MSSA CC398-t571. Antibiotics. 2022;11(12):1755. doi:10.3390/antibiotics11121755
  • Stanaway S, Johnson D, Moulik P, et al. Methicillin-resistant Staphylococcus aureus (MRSA) isolation from diabetic foot ulcers correlates with nasal MRSA carriage. Diabetes Res Clin Pract. 2006;75:47–50. doi:10.1016/j.diabres.2006.05.021
  • Moulik PK, Mtonga R, Gill GV. Amputation and mortality in new-onset diabetic foot ulcers stratified by etiology. Diabetes Care. 2003;26:491–494. doi:10.2337/diacare.26.2.491
  • Fish R, Kutter E, Wheat G, et al. Bacteriophage treatment of intransigent diabetic toe ulcers: a case series. J WOUND CARE. 2016;25:S27–S33. doi:10.12968/jowc.2016.25.7.s27