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Diabetic foot osteomyelitis is usually a consequence of a neglected chronic ulcer, which may produce silent soft tissue infection with contiguous bone involvement . Exploration after ulcer debridement may reveal an exposed bone or joint, which is highly suggestive of osteomyelitis . The clinical suspicion is usually confirmed by radiological investigations (repeated X-rays, magnetic rsonance imaging or computed tomography scans) [3,4]. The optimal management of diabetic osteomyelitis is still a matter of debate and there is no universally accepted strategy [5,6]. One radical option for severe diabetic foot osteomyelitis is surgical amputation, including total ray, transmetatarsal and limb amputation . Lower limb amputations are the most dramatic complications associated with diabetes and are 12-fold more frequent in the diabetic population than in the nondiabetic one . The consequences of amputation are multiple and include psychosocial issues, nonhealing surgical wounds, postoperative infection and postural instability with recurrent ulceration and further amputation . Accordingly, efforts have been made to limit amputation to patients with diabetic foot osteomyelitis . One option is to perform a conservative surgery without local or high-level amputation, followed by prolonged antibiotic therapy [10,11]. Some physicians advocate conservative nonsurgical management of diabetic osteomyelitis . In these cases, it is extremely important to obtain a high-quality specimen for culture and to administrate a long course (several months) of adequate antibiotic therapy. Several sampling techniques are used in clinical practice. Simple swabbing of the ulcer is often performed but should be proscribed because of inaccurate results . Kessler et al.  advocated the use of needle aspiration through the normal skin surrounding the foot ulcer. However, this method was recently shown to be inconsistent with transcutaneous bone biopsy culture . Deep specimens obtained after wound debridement are usually recommended but surgical percutaneous bone biopsy is likely to represent the gold standard method for reliable identification of the causal bacteria . However, because bone biopsy is an expensive and invasive technique that requires an experienced surgeon to carry out the procedure, it is difficult to implement in most health care centres . Furthermore, although Senneville et al.  did not report any side effects with this technique, percutaneous bone biopsy may compromise wound healing in patients with arteriopathy and severe neuropathy.
We evaluated a simplified procedure for the medical management of severe diabetic foot osteomyelitis with exposed bone, based on the results of bone sample culture obtained via the ulcer after a careful debridement of the wound.
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- Materials and Methods
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We evaluated a simplified strategy to manage diabetic osteomyelitis, based on culture results of bone samples obtained via the ulcer after a careful debridement of the wound. The bone sample was taken even if antibiotics prescribed by the general practioner before attendance to our clinic had not been discontinued. Patients received antimicrobials that were effective against the organisms found in the bone culture. Cultures were positive in 97.5% of patients and 88% were considered as cured 6 months after the end of antibiotic therapy.
Of the 54 patients with follow-up data available 1 year after completion of antibiotics and considered as cured at 6 months, there was no relapse of the osteomyelitis. This pragmatic and simplified approach has several advantages: (i) the infected area can be visualized and thus cannot be missed when the specimen is drawn; (ii) the necrotic bone specimen is assumed to have a high bacterial load that may increase the likelihood of positive culture, even with recent antibiotic therapy; (iii) the medical treatment can be quickly implemented after the bone specimen was drawn; and (iv) the method does not create a new wound, which is especially important in patients with severe arteritis.
Our cohort comprised 80 consecutive patients, with most of them having a severe osteomyelitis. Arteritis was associated with difficult to treat osteomyelitis such as calcaneum infections, which are known to have a poor prognosis . Similar to other studies, we found a high frequency of multiresistant bacteria, especially MRSA [11,17,18]. Patients with resistant bacteria had similar risk factors to those reported in other studies, including previous exposure to various antibiotics and frequent hospitalization as a result of complicated diabetes [11,17,18]. This makes the medical treatment of these patients more challenging, in addition to the severity of the disease in our population.
The present study had several limitations. First, the study is observational and retrospective. Second, this simplified approach can be used only in patients with a positive probe-to-bone test and some diabetic patients may have osteomyelitis of the foot with no wound or with a negative probe-to-bone test. However, because the osteomyelitis is usually the result of a neglected chronic ulcer, the rate of a positive probe-to-bone test is high in patients with diabetic osteomyelitis; for example, 95% of the 185 patients with proven diabetic foot osteomyelitis in the series published by Aragon-Sanchez et al. . Third, we cannot exclude contamination of the sample by the skin flora, which may partly explain the high rate of multiresistant bacteria.
Performing a biopsy via an infected open wound is not recommended because of the risk of contamination by colonizing flora. Surgical transcutaneous bone biopsy obtained via a normal skin area after incision has been described by Senneville et al.  and is now the gold standard for microbiological diagnosis . Although the risk of contamination does exist with our approach, we consider the risk to be small for several reasons. First, careful debridement and cleaning of the wound reduces surface contamination. Second, our microbiological results were quite similar to those found by Senneville et al.  and Aragon-Sanchez et al.  who performed surgical bone biopsy and surgical resections, respectively (Table 3). Third, all antibiotic therapy was based on our bone sample culture results and the outcomes were good, taking into account the severity of the osteomyelitis, the high frequency of resistant bacteria and the presence of peripheral arterial disease. At 6 months after antibiotic discontinuation, 65 patients recovered, six had died before assessment and nine were considered as stable or failures.
However, a new episode of infection at a different site and with pathogens distinct from the initial episode occurred in seven patients during the 6-month follow-up period (and six of 54 patients at 1 year). These new distinct episodes of osteomyelitis may be explained by the fact that most of our 80 patients live in a rural, mountainous area, far from the tertiary health care centre . Furthermore, 37.5% of our patients had a past medical history of amputation that may increase the risk of re-ulceration and therefore re-infection at a distinct site.
Most of our patients received an empirical antibiotic therapy administrated by the general practitioners to treat suspected cutaneous infection, usually without any microbiological investigation. Senneville et al.  recommend that patients should not receive any antibiotic therapy for 2–4 weeks before biopsy aiming to avoid false negative results. Indeed, some anti-microbials such as fluoroquinolones or rifampicin may have a prolonged release in bone that may also affect culture results. This recommendation implies a delay in starting definitive treatment. However, all our patients had severe osteomyelitis with perception of a necrotic bone or sequestra on wound exploration. Many of them had a past history of amputation (37.5%) or osteomyelitis (50%) and a majority (60%) had arteritis, which represents the main factor leading to amputation that is associated with infection. Thus, for the vast majority of our diabetic population, we osteomyelitis treatment should not be delayed. Moreover, the bacterial load is likely to be high in sequestra or necrotic bone, whereas the antibiotic penetration in such a bone is weak, especially in arteritic patients. This may increase the efficiency of bone culture despite previous antibiotic therapy. This hypothesis is confirmed in the study by Aragon-Sanchez et al.  in which 71% of patients received antibiotics before the surgical procedure; of 176 bone specimen with histopathological confirmation of bone infection, 20 (11%) were negative for culture, although there was no statistical association between prior antibiotic therapy and negative results in culture.
In conclusion, although surgical transcutaneous bone biopsy obtained via an incision in a normal skin area followed by adequate antibiotic therapy should be the standard of care for treating diabetic osteomyelitis, medical treatment based on the results of cultures of bone sampled via the ulcer after a careful debridement of the wound is an attractive altrenative and is associated with satisfactory outcomes.