640
Views
29
CrossRef citations to date
0
Altmetric
Review

Optimal management of diabetic foot osteomyelitis: challenges and solutions

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 947-959 | Published online: 21 Jun 2019

References

  • Singh N , Armstrong DG , Lipsky BA . Preventing foot ulcers in patients with diabetes. JAMA . 2005;293(2):217–228. doi:10.1001/jama.293.2.217 15644549
  • Boulton AJ , Vileikyte L , Ragnarson-Tennvall G , Apelqvist J . The global burden of diabetic foot disease. Lancet . 2005;366(9498):1719–1724. doi:10.1016/S0140-6736(05)67698-2 16291066
  • Schofield CJ , Libby G , Brennan GM , et al. Mortality and hospitalization in patients after amputation: a comparison between patients with and without diabetes. Diabetes Care . 2006;29(10):2252–2256. doi:10.2337/dc06-0926 17003302
  • Lipsky BA , Berendt AR , Cornia PB , et al. 2012 Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis . 2012;54(12):e132–e173. doi:10.1093/cid/cis346 22619242
  • Pecoraro RE , Ahroni JH , Boyko EJ , Stensel VL . Chronology and determinants of tissue repair in diabetic lower-extremity ulcers. Diabetes . 1991;40(10):1305–1313.1936593
  • Reiber GE , Pecoraro RE , Koepsell TD . Risk factors for amputation in patients with diabetes mellitus. A case-control study. Ann Intern Med . 1992;117(2):97–105.1605439
  • Lavery LA , Armstrong DG , Murdoch DP , Peters EJ , Lipsky BA . Validation of the Infectious Diseases Society of America’s diabetic foot infection classification system. Clin Infect Dis . 2007;44(4):562–565. doi:10.1086/511036 17243061
  • Lipsky BA . Bone of contention: diagnosing diabetic foot osteomyelitis. Clin Infect Dis . 2008;47(4):528–530. doi:10.1086/590012 18611161
  • Lipsky BA , Aragon-Sanchez J , Diggle M , et al. IWGDF guidance on the diagnosis and management of foot infections in persons with diabetes. Diabetes Metab Res Rev . 2016;32(Suppl 1):45–74. doi:10.1002/dmrr.2699 26386266
  • Berendt AR , Peters EJ , Bakker K , et al. Diabetic foot osteomyelitis: a progress report on diagnosis and a systematic review of treatment. Diabetes Metab Res Rev . 2008;24(Suppl 1):S145–S161. doi:10.1002/dmrr.836 18442163
  • Lipsky BA , Berendt AR , Deery HG , et al. Diagnosis and treatment of diabetic foot infections. Clin Infect Dis . 2004;39(7):885–910. doi:10.1086/424846 15472838
  • Lipsky BA . International consensus group on d, treating the infected diabetic f. A report from the international consensus on diagnosing and treating the infected diabetic foot. Diabetes Metab Res Rev . 2004;20(Suppl 1):S68–S77. doi:10.1002/dmrr.453 15150818
  • Yadlapalli N , Vaishnav A , Sheehan P . Conservative management ofdiabetic foot ulcers complicated by osteomyelitis. Wounds . 2002;14:31–35.
  • Embil J . The management of diabetic foot osteomyelitis. Diabetic Foot . 2000;3:76–84.
  • Mutluoglu M , Lipsky BA . Non-surgical treatment of diabetic foot osteomyelitis. Lancet Diabetes Endocrinol . 2017;5(8):668. doi:10.1016/S2213-8587(16)30141-3 28108304
  • Lipsky BA . Treating diabetic foot osteomyelitis primarily with surgery or antibiotics: have we answered the question? Diabetes Care . 2014;37(3):593–595. doi:10.2337/dc13-2510 24558076
  • Molines-Barroso RJ , Lazaro-Martinez JL , Aragon-Sanchez J , Garcia-Morales E , Beneit-Montesinos JV , Alvaro-Afonso FJ . Analysis of transfer lesions in patients who underwent surgery for diabetic foot ulcers located on the plantar aspect of the metatarsal heads. Diabet Med . 2013;30(8):973–976. doi:10.1111/dme.12202 23600614
  • Embil JM , Rose G , Trepman E , et al. Oral antimicrobial therapy for diabetic foot osteomyelitis. Foot Ankle Int . 2006;27(10):771–779. doi:10.1177/107110070602701003 17054876
  • Hartemann-Heurtier A , Senneville E . Diabetic foot osteomyelitis. Diabetes Metab . 2008;34(2):87–95. doi:10.1016/j.diabet.2007.09.005 18242114
  • Henke PK , Blackburn SA , Wainess RW , et al. Osteomyelitis of the foot and toe in adults is a surgical disease: conservative management worsens lower extremity salvage. Ann Surg . 2005;241(6):885–92; discussion 92–4.
  • Aragon-Sanchez J , Lipsky BA . Modern management of diabetic foot osteomyelitis. The when, how and why of conservative approaches. Expert Rev Anti Infect Ther . 2018;16(1):35–50. doi:10.1080/14787210.2018.1417037 29231774
  • Lazaro-Martinez JL , Aragon-Sanchez J , Garcia-Morales E . Antibiotics versus conservative surgery for treating diabetic foot osteomyelitis: a randomized comparative trial. Diabetes Care . 2014;37(3):789–795. doi:10.2337/dc13-1526 24130347
  • Zeun P , Gooday C , Nunney I , Dhatariya K . Predictors of outcomes in diabetic foot osteomyelitis treated initially with conservative (nonsurgical) medical management: a retrospective study. Int J Low Extrem Wounds . 2016;15(1):19–25. doi:10.1177/1534734615596892 26315897
  • Acharya S , Soliman M , Egun A , Rajbhandari SM . Conservative management of diabetic foot osteomyelitis. Diabetes Res Clin Pract . 2013;101(3):e18–e20. doi:10.1016/j.diabres.2013.06.010 23850116
  • Game FL , Jeffcoate WJ . Primarily non-surgical management of osteomyelitis of the foot in diabetes. Diabetologia . 2008;51(6):962–967. doi:10.1007/s00125-008-0976-1 18385975
  • Lesens O , Desbiez F , Vidal M , et al. Culture of per-wound bone specimens: a simplified approach for the medical management of diabetic foot osteomyelitis. Clin Microbiol Infect . 2011;17(2):285–291. doi:10.1111/j.1469-0691.2010.03194.x 20156216
  • Pittet D , Wyssa B , Herter-Clavel C , Kursteiner K , Vaucher J , Lew PD . Outcome of diabetic foot infections treated conservatively: a retrospective cohort study with long-term follow-up. Arch Intern Med . 1999;159(8):851–856.10219931
  • Senneville E , Lombart A , Beltrand E , et al. Outcome of diabetic foot osteomyelitis treated nonsurgically: a retrospective cohort study. Diabetes Care . 2008;31(4):637–642. doi:10.2337/dc07-1744 18184898
  • Valabhji J , Oliver N , Samarasinghe D , Mali T , Gibbs RG , Gedroyc WM . Conservative management of diabetic forefoot ulceration complicated by underlying osteomyelitis: the benefits of magnetic resonance imaging. Diabet Med . 2009;26(11):1127–1134. doi:10.1111/j.1464-5491.2009.02828.x 19929991
  • Jordano-Montanez Q , Muniz-Tatay M , Viade-Julia J , et al. [Diabetic foot osteomyelitis: is conservative treatment possible?]. Enferm Infecc Microbiol Clin . 2014;32(9):555–559. doi:10.1016/j.eimc.2014.03.012 24913994
  • Alfadda A , Malabu UH , El-Desouki MI , et al. Treatment of Graves’ hyperthyroidism–prognostic factors for outcome. Saudi Med J . 2007;28(2):225–230.17268701
  • Malabu UH , Al-Rubeaan KA , Al-Derewish M . Diabetic foot osteomyelitis: usefulness of erythrocyte sedimentation rate in its diagnosis. West Afr J Med . 2007;26(2):113–116.17939311
  • Ertugrul BM , Savk O , Ozturk B , Cobanoglu M , Oncu S , Sakarya S . The diagnosis of diabetic foot osteomyelitis: examination findings and laboratory values. Med Sci Monit . 2009;15(6):CR307–CR312.19478702
  • Waldvogel FA , Medoff G , Swartz MN . Osteomyelitis: a review of clinical features, therapeutic considerations and unusual aspects. 3. Osteomyelitis associated with vascular insufficiency. N Engl J Med . 1970;282(6):316–322. doi:10.1056/NEJM197002052820606 4987436
  • Conterno LO , Da Silva Filho CR . Antibiotics for treating chronic osteomyelitis in adults. Cochrane Database Syst Rev . 2009;3:CD004439.
  • Spellberg B , Lipsky BA . Systemic antibiotic therapy for chronic osteomyelitis in adults. Clin Infect Dis . 2012;54(3):393–407. doi:10.1093/cid/cir842 22157324
  • Senneville E , Robineau O . Treatment options for diabetic foot osteomyelitis. Expert Opin Pharmacother . 2017;18(8):759–765. doi:10.1080/14656566.2017.1316375 28406331
  • Lavigne JP , Sotto A . Microbial management of diabetic foot osteomyelitis. Future Microbiol . 2017;12:1243–1246. doi:10.2217/fmb-2017-0174 28972392
  • Venkatesan P , Lawn S , Macfarlane RM , Fletcher EM , Finch RG , Jeffcoate WJ . Conservative management of osteomyelitis in the feet of diabetic patients. Diabet Med . 1997;14(6):487–490. doi:10.1002/(SICI)1096-9136(199706)14:6<487::AID-DIA373>3.0.CO;2-Q 9212316
  • Senneville E , Yazdanpanah Y , Cazaubiel M , et al. Rifampicin-ofloxacin oral regimen for the treatment of mild to moderate diabetic foot osteomyelitis. J Antimicrob Chemother . 2001;48(6):927–930.11733482
  • Boselli E , Allaouchiche B . [Diffusion in bone tissue of antibiotics]. Presse Med . 1999;28(40):2265–2276.10636023
  • Tone A , Nguyen S , Devemy F , et al. Six-week versus twelve-week antibiotic therapy for nonsurgically treated diabetic foot osteomyelitis: a multicenter open-label controlled randomized study. Diabetes Care . 2015;38(2):302–307. doi:10.2337/dc14-1514 25414157
  • van Asten SAV , Mithani M , Peters EJG , La Fontaine J , Kim PJ , Lavery LA . Complications during the treatment of diabetic foot osteomyelitis. Diabetes Res Clin Pract . 2018;135:58–64. doi:10.1016/j.diabres.2017.06.002 28951333
  • Vouillarmet J , Moret M , Morelec I , Michon P , Dubreuil J . Application of white blood cell SPECT/CT to predict remission after a 6 or 12 week course of antibiotic treatment for diabetic foot osteomyelitis. Diabetologia . 2017;60(12):2486–2494. doi:10.1007/s00125-017-4417-x 28866726
  • Allahabadi S , Haroun KB , Musher DM , Lipsky BA , Barshes NR . Consensus on surgical aspects of managing osteomyelitis in the diabetic foot. Diabet Foot Ankle . 2016;7:30079. doi:10.3402/dfa.v7.30079 27414481
  • Van GH , Siney H , Danan JP , Sachon C , Grimaldi A . Treatment of osteomyelitis in the diabetic foot: contribution of conservative surgery. Diabetes Care . 1996;19(11):1257–1260.8908390
  • Aragon-Sanchez J , Lazaro-Martinez JL , Alvaro-Afonso FJ , Molines-Barroso R . Conservative surgery of diabetic forefoot osteomyelitis: how can i operate on this patient without amputation? Int J Low Extrem Wounds . 2015;14(2):108–131. doi:10.1177/1534734614550686 25256285
  • Lipsky BA , Berendt AR , Cornia PB , et al. 2012 infectious diseases society of america clinical practice guideline for the diagnosis and treatment of diabetic foot infections. J Am Podiatr Med Assoc . 2013;103(1):2–7.23328846
  • Aragon-Sanchez J . Treatment of diabetic foot osteomyelitis: a surgical critique. Int J Low Extrem Wounds . 2010;9(1):37–59. doi:10.1177/1534734610361949 20207622
  • Aragon-Sanchez FJ , Cabrera-Galvan JJ , Quintana-Marrero Y , et al. Outcomes of surgical treatment of diabetic foot osteomyelitis: a series of 185 patients with histopathological confirmation of bone involvement. Diabetologia . 2008;51(11):1962–1970. doi:10.1007/s00125-008-1131-8 18719880
  • Piaggesi A , Schipani E , Campi F , et al. Conservative surgical approach versus non-surgical management for diabetic neuropathic foot ulcers: a randomized trial. Diabet Med . 1998;15(5):412–417. doi:10.1002/(SICI)1096-9136(199805)15:5<412::AID-DIA584>3.0.CO;2-1 9609364
  • Aragon-Sanchez J , Lazaro-Martinez JL , Hernandez-Herrero C , et al. Does osteomyelitis in the feet of patients with diabetes really recur after surgical treatment? Natural history of a surgical series. Diabet Med . 2012;29(6):813–818. doi:10.1111/j.1464-5491.2011.03528.x 22151429
  • Atway S , Nerone VS , Springer KD , Woodruff DM . Rate of residual osteomyelitis after partial foot amputation in diabetic patients: a standardized method for evaluating bone margins with intraoperative culture. J Foot Ankle Surg . 2012;51(6):749–752. doi:10.1053/j.jfas.2012.06.017 22819618
  • Tan JS , Friedman NM , Hazelton-Miller C , Flanagan JP , File TM Jr. Can aggressive treatment of diabetic foot infections reduce the need for above-ankle amputation? Clin Infect Dis . 1996;23(2):286–291.8842265
  • Fujii M , Terashi H , Yokono K . Surgical treatment strategy for diabetic forefoot osteomyelitis. Wound Repair Regen . 2016;24(2):447–453. doi:10.1111/wrr.12418 26844669
  • Shaikh N , Vaughan P , Varty K , Coll AP , Robinson AH . Outcome of limited forefoot amputation with primary closure in patients with diabetes. Bone Joint J . 2013;95-B(8):1083–1087. doi:10.1302/0301-620X.95B8.31280 23908424
  • Widatalla AH, Mahadi SE, Shawer MA, Mahmoud SM, Abdelmageed AE, Ahmed ME. Diabetic foot infections with osteomyelitis: efficacy of combined surgical and medical treatment.Diabet Foot Ankle 2012;3:1. doi:10.3402/dfa.v3i0.18809.
  • Garcia-Morales E , Lazaro-Martinez JL , Aragon-Sanchez J , Cecilia-Matilla A , Garcia-Alvarez Y , Beneit-Montesinos JV . Surgical complications associated with primary closure in patients with diabetic foot osteomyelitis. Diabet Foot Ankle . 2012;3:1. doi:10.3402/dfa.v3i0.19000.
  • Tardaguila-Garcia A , Sanz-Corbalan I , Molines-Barroso RJ , Alvaro-Afonso FJ , Garcia-Alvarez Y , Lazaro-Martinez JL . Complications associated with the approach to metatarsal head resection in diabetic foot osteomyelitis. Int Wound J . 2019;16(2):467–472.
  • Lesens O , Desbiez F , Theis C , et al. Staphylococcus aureus-related diabetic osteomyelitis: medical or surgical management? A French and Spanish retrospective cohort. Int J Low Extrem Wounds . 2015;14(3):284–290. doi:10.1177/1534734614559931 25515373
  • Game F , Jeffcoate W . MRSA and osteomyelitis of the foot in diabetes. Diabet Med . 2004;21(Suppl 4):16–19. doi:10.1111/j.1464-5491.2004.1424-8.x 15315521
  • Widatalla AH , Mahadi SE , Shawer MA , Mahmoud SM , Abdelmageed AE , Ahmed ME . Diabetic foot infections with osteomyelitis: efficacy of combined surgical and medical treatment. Diabetic Foot Ankle . 2012;3:18809. doi:10.3402/dfa.v3i0.18809
  • Sagray BA , Malhotra S , Steinberg JS . Current therapies for diabetic foot infections and osteomyelitis. Clin Podiatr Med Surg . 2014;31(1):57–70. doi:10.1016/j.cpm.2013.09.003 24296018
  • Richard JL , Lavigne JP , Sotto A . Diabetes and foot infection: more than double trouble. Diabetes Metab Res Rev . 2012;28(Suppl 1):46–53. doi:10.1002/dmrr.2234 22271723
  • Bakker K , Schaper NC ; International Working Group on Diabetic Foot Editorial B. The development of global consensus guidelines on the management and prevention of the diabetic foot 2011. Diabetes Metab Res Rev . 2012;28(Suppl 1):116–118. doi:10.1002/dmrr.2254 22271736
  • Game FL . Osteomyelitis in the diabetic foot: diagnosis and management. Med Clin North Am . 2013;97(5):947–956. doi:10.1016/j.mcna.2013.03.010 23992902
  • Cruciani M , Lipsky BA , Mengoli C , de Lalla F . Granulocyte-colony stimulating factors as adjunctive therapy for diabetic foot infections. Cochrane Database Syst Rev . 2013;8:CD006810.23955465
  • Dumville JC , Hinchliffe RJ , Cullum N , et al. Negative pressure wound therapy for treating foot wounds in people with diabetes mellitus. Cochrane Database Syst Rev . 2013;10:CD010318.24132761
  • Cruciani M , Lipsky BA , Mengoli C , de Lalla F . Granulocyte-colony stimulating factors as adjunctive therapy for diabetic foot infections. Cochrane Database Syst Rev . 2009;3:CD006810.19588405
  • Margolin L , Gialanella P . Assessment of the antimicrobial properties of maggots. Int Wound J . 2010;7(3):202–204. doi:10.1111/j.1742-481X.2010.00234.x 20455959
  • Sun X , Jiang K , Chen J , et al. A systematic review of maggot debridement therapy for chronically infected wounds and ulcers. Int J Infect Dis . 2014;25:32–37. doi:10.1016/j.ijid.2014.03.1397 24841930
  • Edwards J , Stapley S . Debridement of diabetic foot ulcers. Cochrane Database Syst Rev . 2010;1:CD003556.20091547
  • Barth RE , Vogely HC , Hoepelman AI , Peters EJ . ‘To bead or not to bead?’ Treatment of osteomyelitis and prosthetic joint-associated infections with gentamicin bead chains. Int J Antimicrob Agents . 2011;38(5):371–375. doi:10.1016/j.ijantimicag.2011.03.008 21549570
  • Roeder B , Van Gils CC , Maling S . Antibiotic beads in the treatment of diabetic pedal osteomyelitis. J Foot Ankle Surg . 2000;39(2):124–130.10789104
  • Kumari S , Harjai K , Chhibber S . Efficacy of bacteriophage treatment in murine burn wound infection induced by klebsiella pneumoniae. J Microbiol Biotechnol . 2009;19(6):622–628.19597322
  • Mendes JJ , Leandro C , Mottola C , et al. In vitro design of a novel lytic bacteriophage cocktail with therapeutic potential against organisms causing diabetic foot infections. J Med Microbiol . 2014;63(Pt 8):1055–1065. doi:10.1099/jmm.0.071753-0 24869663
  • Panagopoulos P , Drosos G , Maltezos E , Papanas N . Local antibiotic delivery systems in diabetic foot osteomyelitis: time for one step beyond? Int J Low Extrem Wounds . 2015;14(1):87–91. doi:10.1177/1534734614566937 25604011
  • Markakis K , Faris AR , Sharaf H , Faris B , Rees S , Bowling FL . Local antibiotic delivery systems: current and future applications for diabetic foot infections. Int J Low Extrem Wounds . 2018;17(1):14–21. doi:10.1177/1534734618757532 29458291
  • Senneville E , Melliez H , Beltrand E , et al. Culture of percutaneous bone biopsy specimens for diagnosis of diabetic foot osteomyelitis: concordance with ulcer swab cultures. Clin Infect Dis . 2006;42(1):57–62. doi:10.1086/498112 16323092
  • Richard JL , Lavigne JP , Got I , et al. Management of patients hospitalized for diabetic foot infection: results of the French OPIDIA study. Diabetes Metab . 2011;37(3):208–215. doi:10.1016/j.diabet.2010.10.003 21169044
  • Schaper NC , Apelqvist J , Bakker K . Reducing lower leg amputations in diabetes: a challenge for patients, healthcare providers and the healthcare system. Diabetologia . 2012;55(7):1869–1872. doi:10.1007/s00125-012-2588-z 22622617
  • Molines-Barroso RJ , Lazaro-Martinez JL , Alvaro-Afonso FJ , Sanz-Corbalan I , Garcia-Klepzig JL , Aragon-Sanchez J . Validation of an algorithm to predict reulceration in amputation patients with diabetes. Int Wound J . 2017;14(3):523–528. doi:10.1111/iwj.12639 27502469
  • Aragon-Sanchez J . Seminar review: a review of the basis of surgical treatment of diabetic foot infections. Int J Low Extrem Wounds . 2011;10(1):33–65. doi:10.1177/1534734611400259 21444608
  • Armstrong DG , Lipsky BA . Diabetic foot infections: stepwise medical and surgical management. Int Wound J . 2004;1(2):123–132. doi:10.1111/j.1742-4801.2004.00035.x 16722884
  • Lazaro-Martinez JL , Aragon-Sanchez J , Alvaro-Afonso FJ , Garcia-Morales E , Garcia-Alvarez Y , Molines-Barroso RJ . The best way to reduce reulcerations: if you understand biomechanics of the diabetic foot, you can do it. Int J Low Extrem Wounds . 2014;13(4):294–319. doi:10.1177/1534734614549417 25256280