554282

research-article2014

IJLXXX10.1177/1534734614554282The International Journal of Lower Extremity WoundsSenneville and Nguyen

Original Review

Difficult Situations Managing Diabetic Foot. Evidences and Personal Views: Is to Operate on Patients With Diabetic Foot Osteomyelitis Old-Fashioned?

The International Journal of Lower Extremity Wounds 2014, Vol. 13(4) 241­–246 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1534734614554282 ijl.sagepub.com

Eric Senneville, MD, PhD1 and Sophie Nguyen, MD1

Abstract Both medical and surgical approaches have been shown to be effective in the treatment of patients with diabetic foot osteomyelitis (DFO). In patients with risk factors of bad outcome such as major bone destruction, concomitant acute infections requiring drainage, problems in limb perfusion, highly resistant bacteria, and contraindication for or patient refusal of prolonged antibiotic therapy, the choice of surgery does not require further discussion. On the contrary, modest changes of bone on imaging assessment and no limiting factors as described above make medical treatment an attractive option for patients with DFO provided the rules of antibiotic treatment of chronic osteomyelitis are respected. The key question may not be to oppose surgery and medical treatment but to identify patients who need surgery and those who do not. There is currently no classification or score system that may allow physician to decide whether medical or surgical approach is best adapted to a given patient, and so both experience and skill of the multidisciplinary team appear paramount for guiding the choice of the best adapted (“tailored”) strategy in a given patient. In this regard, it would be interesting to compare surgical and medical approaches for DFO that apparently may benefit from one or another (ie, bone lesions seen on plain radiographs of the foot but without bone fragmentation or multiple sites of osteomyelitis, no contraindication to prolonged antibiotic therapy, and location of bone involvement that may allow conservative surgery). Given the current available data on the therapeutic options of DFO, it appears that surgery for those patients is obviously not an old-fashioned option. Keywords diabetic foot osteomyelitis, antibiotic treatment, surgery

Classification Over half of chronic diabetic foot wounds are complicated by soft tissue infection that may involve underlying osteoarticular structures in 20% to 60% of the cases according to infection severity.1-4 These infections, designated by the term diabetic foot osteomyelitis (DFO), are difficult to treat and are associated with increased risk of relapsing infection, hospitalization episodes, and foot amputations.5 The management of DFO is one of the most conflicting aspects of diabetic foot infection.6-10 As for other types of osteomyelitis, the main limitation of the management of such infections is the very large diversity of the situations encountered by physicians. We aimed to review the currents advances in the knowledge regarding the place of medical or surgical approaches for the treatment of DFO. Osteomyelitis is defined as an inflammatory process in bone that affects any part of the foot located under the malleoli in a patient with diabetes mellitus. DFO is mostly, if not exclusively, the consequence of a soft tissue infection

that spreads to the underlying osteoarticular structures. DFO can also result from either penetrating injury or ischemic soft tissue loss.11,12 A surgical study has proposed to classify DFO into 3 types according to the histopathological findings (acute, chronic, and acute exacerbation of chronic osteomyelitis).13 More recently, the same team proposed to separate DFO into 4 classes by including some clinical aspects: osteomyelitis without ischemia and without soft tissue involvement (class 1), osteomyelitis with ischemia without soft tissue involvement (class 2), osteomyelitis with soft tissue involvement (class 3), and osteomyelitis with ischemia and soft tissue involvement (class 4).14 This study showed a 1

Gustave Dron Hospital, Tourcoing, France

Corresponding Author: Eric Senneville, Infectious Diseases Department, Gustave Dron Hospital, 135 rue du Président Coty, 59200 Tourcoing, France. Email: [email protected]

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statistically significant trend toward increased severity (ie, from class I to class IV) and the risk of both limb amputation and mortality. However, this classification appears more useful for conducting clinical research studies than to help physicians choose the most appropriate treatment strategy for a given patient since the diagnosis of deep tissue infection associated with DFO may be difficult before surgery.

Microbiology Microbiology of DFO is usually polymicrobial,15 and in almost all the reported series, Staphylococcus aureus is the most common pathogen cultured from bone samples.16-18 Other Gram-positive cocci frequently isolated from bone samples are S epidermidis, beta-hemolytic streptococci, and diphteroids. Among the enterobacteriaceae, Escherichia coli, Klebsiella pneumoniae, and Proteus spp are the most common pathogens followed by Pseudomonas aeruginosa. The number of obligate anaerobes (mostly Finegoldia magna) depends on the method of sampling and transportation of the bone fragments. The increased prevalence of multiresistant bacteria (especially methicillin-resistant S aureus [MRSA] and extended spectrum beta-lactamaseproducing Gram-negative bacilli, even carbapenem-resistant enterobacteriaceae) has been reported in patients with DFO.19,20 Importantly, bacteria involved in DFO come from the surface, but bacteria present in the superficial tissues may largely differ from those infecting deeper layers, especially bones.21

Surgical Approach Surgery is needed in DFO for the control of concomitant deep infection when required. It consists in draining pus and removing economically all necrotic tissues, in order to reduce the bacterial inoculum and remove the biofilm and hence the bacteria included in it, which is essential for the antibiotic therapy to be effective. Because of the complexity of these infections, which require simultaneous control of the vascular status of the limb, determination of the best level of amputation, and the possibility of covering the dehiscence due to resection, such patients should necessarily be placed in the hands of the most interested and experienced surgeons in these situations.22 Surgery has been long considered essential to ease the action of the antibiotic therapy even to replace them given the poor results obtained by antibiotics alone in the treatment of DFO. In this regard, removing the entire infected bone has been considered in the past and even recently as the standard treatment.23 Indeed, DFO cumulates many risk factors for failure, such as (a) the micro- and macro-vascular complications that may compromise blood supply to the infected tissues of the foot in these patients and (b) the chronic nature of bone

infection that affects the cortical part, which is generally considered more difficult to sterilize than the medullar part and which involves bacteria likely to be in slow metabolism phases and thus may exhibit an adaptive resistance to most antibiotics. Staphylococci, especially S aureus, can form a biofilm in which they may escape to specific and innate immune responses.24 The immunological alterations described in diabetic patients have not been strongly linked to the occurrence of infections, and their negative role in the outcome of patients with DFO has not been clearly established. Finally, highly resistant bacteria particularly enterobacteriaceae and intolerance to some antibiotics due to organ dysfunction, especially renal and hepatic or drug– drug interactions, are other potential limitations of the medical approach of DFO. All the potential weaknesses of the antibiotic therapy of DFO have led to the considering of surgery (ie, minor or major amputations and resection of the infected bone tissues) as the primary choice for these patients. Surgery is rapidly effective in reducing the bacterial load at the infected site, can remove necrotic tissues that cannot be attainable (and treatable) by antibiotics, and may also be prophylactic in that it can correct the bone deformity at the origin of the foot ulcer that led to the osteomyelitis.13,23,25-27 The effectiveness of surgery in reducing the recurrence of osteomyelitis has been evaluated in a single prospective study that enrolled 74 evaluable patients with DFO.26 Patients were treated with conservative surgery (59.3%), minor amputations (39.5%), and major amputation (1.2%) with a postoperative antibiotic treatment for a median period of 36 days. Reoperation was required because of persistent infection in 24.7% of the patients. After a mean follow-up duration of 101.8 weeks, wound healing was achieved for a median of 8 weeks among the 65 patients evaluable for follow-up after healing. Although recurrence and new episodes of osteomyelitis were only recorded in, respectively, 4.6% and 16.9% of the patients, reulcerations were seen in 43% of the patients.26 Conservative surgery for DFO, which consists in removing the bone infection while avoiding amputation, is an attractive option.27,28 Ha Van et al showed that limited resection of the infected phalanx or metatarsal bone under the wound, together with removal of the ulcer site, was effective to obtain complete wound healing.27 Aragón-Sánchez et al reported a consecutive series of 185 diabetic patients with osteomyelitis of the foot and histopathological confirmation of bone involvement, all treated surgically, including 91 conservative surgical procedures.13 The risks of failure in the case of conservative surgery were exposed bone, the presence of ischemia, and necrotizing soft tissue infection. Conservative surgery was successful in almost half of the cases. Tan and colleagues found that an aggressive surgical approach against foot infection, including osteomyelitis, in

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Senneville and Nguyen hospitalized diabetic patients was associated with a 13% rate of above-ankle amputation.29 Other authors have suggested that prompt toe amputation is a cost-effective solution,30 but this approach has not been clearly evaluated in large-scale reports. Another potential advantage of the conservative surgery is to allow the reduction of the duration of the antibiotic therapy.27

Medical Approach The main advantage of treating DFO medically is (a) it does not induce biomechanical changes that may occur after surgical procedures, (b) it avoids potential medical/surgical complications of surgical procedures, and (c) it may be a better cost-effective approach although the latter argument has not been clearly demonstrated.19 Microbiological documentation appears of paramount importance in patients with DFO treated medically as the chances to achieve a remission of osteomyelitis only depend on the efficacy of the antibiotic therapy. This is less true in the setting of surgical approach of DFO as all the infected bone material that has been removed does not need any antibiotic and as most antibiotics are capable of arresting the infection in the residual (nonnecrotic) infected bone. The identification of the infecting pathogens in DFO is a subject of debate. It is a major step during any sort of chronic osteomyelitis that helps provide patients with the best adapted antimicrobial treatment. In the setting of DFO, it has been shown that the concordance between cultures results of superficial soft tissue samples (swabs or needle aspiration) and bone sample (bone biopsy) was low, well below 50%.17,31-33 The overall concordance between swabs and transcutaneous bone biopsy was only 23.9%, with S aureus showing the strongest correlation (46.7%) as was reported by Mackowiak et al in nondiabetic chronic osteomyelitis.17,34 The higher concordance obtained for S aureus in DFO between superficial and deeper samples’ culture results may explain why some studies have defended the interest of swab cultures for the bacterial documentation of DFO.30 The results of a recent retrospective study suggest that deep wound cultures correlate well with bone cultures.21 However, in this study 11/25 patients (44%) had no strict similarity between superficial and deeper samples, which was potentially responsible for over- or undertreating osteomyelitis in these cases. Although it permits to affirm the existence of bone infection, histopathology testing of bone samples has been shown be difficult in interpretation and does not provide better diagnostic information than a microbiological study.35,36 The main advantage of bone biopsy is finally to provide reliable data on the causative organisms and to determine their profile of susceptibility to antimicrobial agents.37 Current data suggest that percutaneous bone biopsy (Figure 1) in patients with a suspicion of DFO and without

Figure 1.  Percutaneous bone biopsy. Courtesy of Dr Eric Beltrand.

need for surgery of the foot appears to be the most appropriate method to obtain a definite diagnosis and a reliable microbiological documentation of DFO.38 Despite favorable results established in recent studies, transcutaneous bone biopsy has not been implemented in the routine practice of most diabetic foot centers.39 In addition, it is usually thought that this technique may result in introducing bacteria in bone or fracturing the biopsied bone, although these complications have not been reported by the teams using routinely this technique.17,18,40 Antibiotic therapy chosen on the basis of nonbone tissues (swabs or deeper samples) and prescribed for longer durations than for soft tissue infection has been classically used by physicians involved in the management of such patients with apparently good results.10,41 However, these studies were retrospective and did not include a sufficient posttreatment follow-up (ie, at least 1 year) that could allow detection of late relapsing episodes of DFO. Another approach is to consider that DFO should be treated like any other chronic osteomyelitis. It is widely admitted that a reliable bacterial documentation should be obtained in patients with chronic osteomyelitis (other than DFO) in order to best prescribe antibiotic regimens comprising agents with high bone/biofilm diffusion and sustained activity against bacteria in stationary-growth phase as seen in these chronic infections.42 Antibiotics exhibiting such properties are limited to rifampicin, fluoroquinolones, clindamycin, linezolid, and daptomycin. The propensity of these antibiotics to select the resistant mutants present naturally in the offending bacterial population requires prescribing these agents in combination, especially rifampicin, in an attempt to prevent the emergence of these mutants.43 This represents a strong argument for obtaining a reliable identification of the offending pathogens and their susceptibility profile to antibiotics when the prescription of such antibiotics is considered. Nevertheless, despite attempts to provide such patients

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with most adapted antibiotic treatment, it has not been clearly demonstrated that this approach improves the outcome of patients with DFO.38 In a multicenter retrospective cohort study of 50 consecutive patients diagnosed with DFO and managed with antibiotic therapy alone, remission was recorded in 32 (64%) patients.44 The remission rate assessed at the end of a posttreatment follow-up of at least 12 months was 81.2% in the group of 22 patients treated with rifampicin combinations on the basis of bone culture results versus 50% in the group treated according to the results of superficial samples (P = .04).44 The medical approach has some limitations: (a) the prolonged antibiotic treatment, which is likely associated with drug-related side-effects, including Clostridium difficile diarrhea and the emergence of antibiotic resistant organisms, in particular MRSA and resistant Gram-negative bacilli; (b) the risk of relapsing infections due to the persistence of the infected bone tissues, the sterilization of which can never be affirmed; and (c) the persistence of bone deformity at the origin of the foot ulcer that allows the bacteria to reach and infect the underlying osteoarticular structures. It has also been stated that failure of medical treatment of DFO could be associated with a more proximal level of amputation when compared to surgical treatment.28

Medical Versus Surgical Approaches The comparison of results established by studies that assessed medical versus surgical therapy for DFO is difficult since surgery and antibiotic treatments as well as definition criterion and endpoints used by the authors are not identical from one study to another. In addition, compared to medical studies, patients included in surgical studies are likely to have more severe infection and/or more risk factors of bad outcome like necrosis, ischemia, or concomitant soft tissue infections, which augment the need for amputation, and are associated with increased time to healing.13,26 Studies on surgical treatment of DFO usually did not comprise prolonged clinical and radiological assessment after the end of treatment in order to record relapsing infections as recommended for any other sort of chronic osteomyelitis. In addition, the daily doses, mode of administration, and the type of antibiotic used were not optimal in the series of patients published so far. The medical approach cannot be proposed to every patient with DFO as some requirements are necessary for the antibiotic therapy to achieve satisfactory results. It is essential that (a) the blood supply to the infected foot would be satisfactory, (b) the offending pathogens are susceptible to antibiotics suitable for the treatment of chronic osteomyelitis, (c) the patient has no contraindication to these antibiotics, and (d) the severity of the bone destruction does not impair the chances to obtain a remission of the bone infection. The latter requirement is probably the one that is the

most difficult to assess. It is generally thought that necrotic infected bone cannot correctly be treated since antibiotics are unable to achieve sufficient concentration levels in it, but it is difficult in the routine practice to affirm that the osteomyelitis process involves necrotic or viable bone issues. Ha Van and colleagues compared the outcome of patients with DFO treated medically or surgically. Surgical patients had conservative surgery associated with antibiotics, whereas medical patients only received antibiotics.27 The authors concluded that conservative surgery contributes to an increase in the healing rate of foot ulcers with osteomyelitis compared with a medical treatment alone; the healing rate was 57% in the group treated by the medical treatment alone versus 78% in the surgical group (P < .008), and the duration of healing was, respectively, 462 ± 98 days versus 181 ± 30 days (P < .008). The authors stated that the poor penetration of antibiotics in infected bone tissues could explain their poor efficacy in osteomyelitis, but it must be noted that most patients were treated with beta-lactam agents, which are not best adapted for the treatment of chronic osteomyelitis, by oral route (which exposes to suboptimal blood levels and consequently to low tissue levels since these antibiotics have a low oral bioavailability) and were selected on the basis of superficial samples (which do not identify reliably the offending bone pathogens). Surgical patients were compared to a historical cohort of patients treated medically. Despite these important limitations, it must be noted that this study was the first one to compare the efficacy of medical versus surgical approaches in patients with DFO. Tan and colleagues reported a lower rate of above-ankle amputation in patients who underwent debridement or local limited amputation than in patients treated with antibiotic therapy alone, and a shorter hospital stay.29 In a retrospective study of 147 patients with DFO, Game and Jeffcoate found that 113 patients treated with antibiotic therapy alone were operated for a limb amputation (major in 6 patients and minor in 28 patients).19 Remission rates were similar in both surgical and medical groups (78.6% and 83.3%, respectively). In a smaller size retrospective study, patients with DFO treated with antibiotic therapy alone (n = 15) were shown to have similar outcome than patients who underwent minor amputation (n = 22).45 In this study, duration of hospitalization stay, antibiotic therapy, and wound healing were also comparable. Recently, Lázaro-Martínez et al reported the results of a prospective study that aimed to compare the outcomes of patients with DFO treated with antibiotics alone versus patients who underwent conservative surgery. At the end of a posttreatment follow-up of 12 weeks, 18 patients (75%) achieved primary healing in the medical group versus 19 (86.3%) in the surgical group (P = .33).46 No difference was found between the 2 groups regarding time to healing (7 vs 6 weeks) and minor amputations (P = .336). The authors

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Senneville and Nguyen concluded that antibiotics and surgical treatment have similar outcomes in terms of healing rates, time to healing, and short-term complications in patients with neuropathic forefoot ulcers complicated by osteomyelitis without ischemia or necrotizing soft tissue infections.46 In summary, although the medical approach has the advantage of patient acceptability and does not imply hospitalization, the surgical approach may be associated with a shorter time to healing of the foot wound and a lower rate of recurrence due to removal of the infected necrotic bone and correction of the foot deformity at the origin of the foot ulcer. The surgical approach for the treatment of DFO, including conservative surgery, may result in biomechanical alterations of the foot, reulceration due to pressure transfer syndrome, and finally to new osteomyelitis episodes contiguous to the initial one. Some patients may be reluctant to the surgical intervention and may prefer the medical option. Another criticism against surgery for DFO concerns the cost–benefit ratio, which appears to be higher for the surgery versus medical treatment although this question has never been addressed specifically in published studies. Both medical and surgical approaches for the treatment of DFO have strengths and weaknesses. Both approaches have been shown effective in the treatment of patients with DFO. In patients with risk factors of bad outcome such as major bone destruction, concomitant acute infections requiring drainage, problems in limb perfusion, highly resistant bacteria, and contraindication for or patient refusal of prolonged antibiotic therapy, the choice of surgery does not require further discussion. On the contrary, modest changes of bone on imaging assessment and no limiting factors as described above make medical treatment an attractive option for patients with DFO provided the rules of antibiotic treatment of chronic osteomyelitis are respected. The key question may not be to oppose surgery and medical treatment but to identify patients who need surgery and those who do not. There is currently no classification or score system that may allow physicians to decide whether medical or surgical approach is best adapted to a given patient, and so both experience and skill of the multidisciplinary team appear paramount for guiding the choice of the best adapted (“tailored”) strategy in a given patient. In this regard, it would be interesting to compare surgical and medical approaches for DFO that apparently may benefit from one or the other option (ie, bone lesions seen on plain radiographs of the foot but without bone fragmentation or multiple sites of osteomyelitis, no contraindication to prolonged antibiotic therapy, and location of bone involvement that may allow conservative surgery). Given the current available data on the therapeutic options of DFO, it appears that surgery for those patients is obviously not an old-fashioned option. Moreover, if the growing bacterial resistance, especially in Gram-negative bacilli and the limitations in the development of antibiotic armamentarium persist and even worsen, surgery should

occupy a prominent place in the management of these patients in the near future. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.

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32. Kessler L, Piemont Y, Ortega F, et al. Comparison of microbiological results of needle puncture vs. superficial swab in infected diabetic foot ulcer with osteomyelitis. Diabet Med. 2006;23:99-102. 33. Senneville E, Morant H, Descamps D, et al. Needle puncture and transcutaneous bone biopsy cultures are inconsistent in patients with diabetes and suspected osteomyelitis of the foot. Clin Infect Dis. 2009;48:888-893. 34. Mackowiak PA, Jones SR, Smith JW. Diagnostic value of sinus-tract cultures in chronic osteomyelitis. JAMA. 1978;239:2772-2775. 35. Weiner RD, Viselli SJ, Fulkert KA, Accetta P. Histology versus microbiology for accuracy in identification of osteomyelitis in the diabetic foot. J Foot Ankle Surg. 2011;50: 197-200. 36. Meyr AJ, Singh S, Zhang X, et al. Statistical reliability of bone biopsy for the diagnosis of diabetic foot osteomyelitis. J Foot Ankle Surg. 2011;50:663-667. 37. Ertugrul MB, Baktiroglu S, Salman S, et al. The diagnosis of osteomyelitis of the foot in diabetes: microbiological examination vs. magnetic resonance imaging and labelled leucocyte scanning. Diabet Med. 2006;23:649-653. 38. 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. 39. 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;37:208-215. 40. Grayson ML, Gibbons GW, Balogh K, Levin E, Karchmer AW. Probing to bone in infected pedal ulcers. A clinical sign of underlying osteomyelitis in diabetic patients. JAMA. 1995;273:721-723. 41. Yadlapalli N, Vaishnar A, Sheehan P. Conservative management of diabetic foot ulcers complicated by osteomyelitis. Wounds. 2002;14:31-35. 42. Zuluaga AF, Galvis W, Jaimes F, Vesga O. Lack of microbiological concordance between bone and nonbone specimens in chronic osteomyelitis: an observational study. BMC Infect Dis. 2002;2:8. 43. Kaye KS, Engemann JJ, Fraimow HS, Abrutyn E. Pathogens resistant to antimicrobial agents: epidemiology, molecular mechanisms and clinical management. Infect Dis Clin North Am. 2004;18:467-511. 44. Senneville E, Lombart A, Beltrand E, et al. Outcome of diabetic foot osteomyelitis treated non-surgically: a retrospective cohort study. Diabetes Care. 2008;31:637-642. 45. Ulcay A, Karakas A, Mutluoglu M, Uzun G, Turhan V, Ay H. Antibiotherapy with and without bone debridement in diabetic foot osteomyelitis: a retrospective cohort study. Pak J Med Sci. 2014;30:28-31. 46. Lázaro-Martínez JL, Aragón-Sánchez J, García-Morales E. Antibiotics versus conservative surgery for treating diabetic foot osteomyelitis: a randomized comparative trial. Diabetes Care. 2014;37:789-795.

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Difficult situations managing diabetic foot. Evidences and personal views: is to operate on patients with diabetic foot osteomyelitis old-fashioned?

Both medical and surgical approaches have been shown to be effective in the treatment of patients with diabetic foot osteomyelitis (DFO). In patients ...
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