OSTEOMYELITIS : REVIEW OF PATHOPHYSIOLOGY, DIAGNOSTIC MODALITIES AND THERAPEUTIC OPTIONS

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1 MISE AU POINT / IN-DEPTH REVIEW OSTEOMYELITIS : REVIEW OF PATHOPHYSIOLOGY, DIAGNOSTIC MODALITIES AND THERAPEUTIC OPTIONS Albert J. EID 1, Elie F. BERBARI 2 Eid AJ, Berbari EF. Osteomyelitis : Review of pathophysiology, diagnostic modalities and therapeutic options. J Med Liban 2012 ; 60 (1) : ABSTRACT : Osteomyelitis can affect every bone and is heterogeneous in its pathophysiology and presentation. When the diagnosis is clinically suspected, further studies such as serum inflammatory markers and imaging studies should be performed. Magnetic resonance imaging can be very useful in establishing the diagnosis and determining the extent of infection. When possible, bone specimens should be obtained and cultured prior to the initiation of antimicrobial therapy. Surgical debridement is often required for chronic or contiguous osteomyelitis for successful eradication of the infection. The ultimate test-of-cure is the lack of clinical relapse after the discontinuation of antimicrobials. INTRODUCTION Osteomyelitis is an infection of the bone and bone marrow. It can involve any bone of the human body and can occur through a variety of mechanisms. The difference in pathophysiology of various types of osteomyelitis mandates specific therapeutic strategies aimed at the eradication of the infection while preserving bone integrity and function. Osteomyelitis can be acute or chronic and may result from hematogenous seeding of the bone, extension of the infection from adjacent soft tissue, or direct inoculation of the bone through skin and soft tissue defects following trauma or surgery. Once established, osteomyelitis leads to progressive softening and necrosis of the bone resulting into the formation of sequestra. At this stage of the disease, surgical debridement becomes a requirement for cure. The presence of hardware at the site of infection is a complicating factor that could compromise treatment success. Despite adequate treatment, failure is not uncommon. Therefore, in order to improve the outcome, clinicians should understand the disease process and gain experience manipulating the treatment tools. Hence, the importance of this review. 1 Division of Infectious Diseases, University of Kansas Medical Center, Kansas City, Kansas; 2 Division of Infectious Diseases, College of Medicine, Mayo Clinic, Rochester, Minnesota, USA. Correspondence: Albert J. Eid, MD. Division of Infectious Diseases. University of Kansas Medical Center, 2067 Delp Rainbow Blvd. Kansas City. KS USA. aeid@kumc.edu Tel.: Eid AJ, Berbari EF. L ostéomyélite : étude approfondie de la pathophysiologie, des modalités diagnostiques et des options thérapeutiques. J Med Liban 2012 ; 60 (1) : RÉSUMÉ : L ostéomyélite peut atteindre tous les os du squelette humain et possède une pathophysiologie et une présentation clinique très hétérogènes. Lorsque le diagnostic est considéré, certains examens doivent être obtenus, notamment les marqueurs d inflammation et des examens radiologiques. L imagerie par résonance magnétique peut être très utile pour confirmer le diagnostic et déterminer l étendue de l infection. Lorsque cela s avère possible, des échantillons osseux doivent être obtenus et cultivés avant le début de l antibiothérapie. Un débridement chirurgical est souvent nécessaire pour l éradication complète de l ostéomyélite chronique ou contiguë. Le test ultime de guérison est l absence de rechute clinique après l arrêt des antibiotiques. Herein, we will address the pathogenesis of osteomyelitis, the available diagnostic modalities, and various therapeutic strategies. Due to the difference in pathophysiology, microbiology, and management, we will separately discuss different entities including osteomyelitis due to open fractures, vertebral osteomyelitis, acute hematogenous osteomyelitis, osteomyelitis in patients with diabetes mellitus and osteomyelitis associated with prosthetic joint infection. A brief overview of osteomyelitis due to some specific pathogens such as Brucella species, Salmonella species, mycobacteria and fungi will also be reviewed. PATHOGENESIS OF OSTEOMYELITIS Experimental animal model of bone infection has revealed that bone is resistant to infection [1]. Osteomyelitis occurs only when a large inoculum of bacteria is introduced into the bone in conjunction with trauma, necrosis, or presence of foreign bodies [2]. Bacteria (i.e. Staphylococcus aureus) adhere to bone matrix via receptors to fibronectin, laminin, collagen and other structural proteins. Microorganisms elude the host defenses and antibiotics through a variety of mechanisms including surviving in a dormant state inside osteoblasts, developing a biofilm, and acquiring a very slow metabolic rate [3-4]. Furthermore, studies in a guinea pig model of post-traumatic osteomyelitis showed significant reduction of leukocyte locomotion after trauma and infection with S. aureus for up to 90 days [5]. The presence of prosthetic material contiguous to bone can lead to specific polymorphonuclear leu- Lebanese Medical Journal 2012 Volume 60 (1) 51

2 kocytes defect and therefore protects bacteria from phagocytosis. Inflammation, resulting from the interaction between bacteria and leukocytes, results in the release of cytokines and the development of osteolysis [3-4]. In patients with acute osteomyelitis of the long bones, it is believed that the metaphysis is the site of predilection due to slow blood flow in the metaphyseal vascular loops and the lack of phagocytic lining cells [6]. Once the infection is established in the metaphysis, the inflammatory exudate leads to increased pressure in the bone and intramedullary canal. Subsequently, the extension of this exudate into the cortex will eventually lead to periosteal elevation or rupture, disrupting the blood flow and causing bone infarction and the formation of an abscess or sequestrum. In chronic osteomyelitis, the inflammation is mild to moderate and little or no ischemic necrosis occurs [4]. The type and site of osteomyelitis is largely determined by the mechanism of infection, the virulence of the infecting organism, and the immune status and comorbid conditions of the patient [6-7] (Table I). Osteomyelitis could develop through hematogenous seeding of the bone from a remote source of infection, extension of the infection from adjacent soft tissue overlying the involved bone; or directly via inoculation of the bone following trauma or surgery. S. aureus is the most commonly isolated organism in osteomyelitis. Other microorganisms such as coagulasenegative staphylococci, aerobic gram-negative bacilli, and anaerobes are frequently encountered as well (Table II). Patients with certain conditions such as immunosuppression, immune diseases (i.e. rheumatoid arthritis), diabetes mellitus, smoking, malnutrition, malignancy, extremes of age, chronic hypoxia, and renal or hepatic failure are at increased risk for osteomyelitis. Other local factors are equally important. Those include chronic edema, peripheral vascular disease, neuropathy, prior surgery, extensive scarring, and radiation fibrosis [6-8]. DIAGNOSIS AND DIAGNOSTIC MODALITIES Osteomyelitis should be suspected when patients present with pain, swelling, erythema or warmth of the skin and soft tissue overlying bone. Subacute or chronic pain is commonly the only manifestation. Systemic symptoms (i.e. fever and chills) are present in patients with acute osteomyelitis but seldom present in patients with chronic osteomyelitis. Draining sinuses are typically seen in cases of chronic osteomyelitis. The presence of exposed bone or prosthetic material for a period of time is highly sug- TABLE I ETIOLOGY OF OSTEOMYELITIS AND UNDERLYING CONDITIONS Mechanism Special groups Etiology Hematogenous osteomyelitis Common in children and adults Staphylococcus aureus Neonates Enterobacteriaceae, Group B streptococci Infants and children* Haemophilus influenzae group B Injection drug users Staphylococcus aureus, Pseudomonas aeruginosa, Candida spp. Vertebral osteomyelitis Most common in adults Staphylococcus aureus Urinary tract infection Aerobic gram-negative bacilli, Enterococcus spp. Injection drug users Pseudomonas aeruginosa, Staphylococcus aureus, Candida spp. Following spine surgery Coagulase-negative staphylococci, Staphylococcus aureus, aerobic gram-negative bacilli Infections of intravascular devices Candida spp. In endemic regions Mycobacterium tuberculosis, Brucella spp. Contiguous focus osteomyelitis Diabetes mellitus, vascular insufficiency, Polymicrobial: Staphylococcus aureus, beta-hemolytic or following a contaminated open fracture streptococci, Enterococcus spp., aerobic gram-negative bacilli Soil contamination Clostridium spp., Bacillus spp., Stenotrophomonas maltophilia, Nocardia spp., atypical mycobacteria, Aspergillus spp., Rhizopus spp., Mucor spp. Orthopedic fixation devices Staphylococcus aureus, coagulase-negative staphylococci Cat bites Pasteurella multocida Following puncture injuries on the foot Pseudomonas aeruginosa by nails or other sharp objects Following periodontal infection Actinomyces spp. *The incidence of osteomyelitis due to Haemophilus influenza type B significantly decreased due to the routine vaccination of children. 52 Lebanese Medical Journal 2012 Volume 60 (1) A.J. EID, E.F. BERBARI Osteomyelitis

3 TABLE II Common Staphylococcus aureus Coagulase-negative staphylococci Streptococci Enterococci Pseudomonas spp. Enterobacter spp. Proteus spp. Escherischia coli Serratia spp. Anaerobes (Peptostreptococcus spp., Clostridium spp., B. fragilis group.) MICROBIOLOGY OF OSTEOMYELITIS Less common Mycobacterium tuberculosis Rapidly growing mycobacteria Mycobacterium avium complex Endemic fungi Candida spp. Aspergillus spp. Mycoplasma spp. Brucella spp. Salmonella spp. Actinomycetes Tropheryma whipplei gestive of osteomyelitis. In fact, the probe-to-bone test is widely used to diagnose osteomyelitis in patients with diabetic foot ulcers and contiguous osteomyelitis. Grayson et al. found that this test has a sensitivity of 66% and a positive predictive value of 89% [9]. The confirmation of osteomyelitis requires the use of a variety of laboratory, microbiologic, radiographic and pathologic tests. Erythrocyte sedimentation rate (ESR) and C-reactive protein (CRP) are usually abnormal. The white blood cell count is occasionally elevated. The platelet count can be elevated (inflammatory marker) while the hemoglobin concentration can be low (anemia of chronic disease). Blood cultures may be positive in acute hematogenous and vertebral osteomyelitis. Cultures of superficial wounds or sinus tracts should be cautiously interpreted and should not be used to guide antimicrobial therapy unless S. aureus is isolated from those cultures [10-11]. In one study, only 44% of the sinus tract cultures grew the same operative pathogen. The isolation of S. aureus from the sinus tract correlated with the presence of S. aureus in the operative specimen. However, less than half of the sinus tract cultures obtained from patients with S. aureus osteomyelitis contained this organism [11]. Bone tissue sampling via needle aspiration under radiologic guidance or surgical procedure allow the identification of the infectious organism and the determination of its in vitro susceptibility profile [6]. The latter information is crucial for the initiation of appropriate and effective antimicrobial therapy (Table III). The bone tissue collected from the infected site can also be submitted for histopathologic examination which is considered the gold standard for the diagnosis of osteomyelitis. Conventional radiography has little value in diagnosing acute osteomyelitis but it might be helpful in cases of chronic osteomyelitis. At least days are needed before abnormalities consistent with osteomyelitis are seen. In one study, the sensitivity of plain radiographs in cases of diabetic foot osteomyelitis was found to be 54%, while the specificity was 68%. The radiographic signs that were considered diagnostic included focal or geographic areas of marrow lucency, loss of cortex with bony erosion, new bone formation, bone sclerosis with or without erosion, sequestration, involucrum, and periosteal elevation [12]. Nuclear bone scans using a variety of radiotracers (Technetium 99m methylene diphosphonate, Galliumcitrate 67, and Indium 111-labeled white blood cells) are commonly used to diagnose osteomyelitis. The performance of those scans varies depending upon the clinical situation [13]. In adults with normal radiographs (no lesions that cause increased bone turnover), the threephase bone scan has higher accuracy than the other scans with 94% sensitivity and 95% specificity. However, when bone remodeling is increased, the specificity of the test decreases to 33% [13]. In presence of osteomyelitis, significant uptake is seen in all three phases of the study (immediately after injection, at 15 minutes and 4 hours) as opposed to increased uptake only in the first two phases in patients with cellulitis. Gallium scans detect the areas of inflammation due to the affinity of gallium-67 to acute phase reactants (i.e. lactoferrin and transferrin) [14]. The results of studies evaluating their sensitivity and specificity are not consistent. When studies are combined together, the overall sensitivity is approximately 81% and the specificity is 69% [13]. Some authors believe that gallium scans have better performance for the evaluation of vertebral osteomyelitis. This is supported by data from one study showing high sensitivity, specificity and accuracy [15]. Tagged white blood cell scans show accumulation of tagged white cells in the bone marrow and at the site of inflammation or infection [14]. In a meta-analysis, the sensitivity of Indium 111-labeled white blood cells scan was 84% for extra-axial chronic osteomyelitis as opposed to only 21% for the axial skeleton. Similarly, the specificity was 80% in the peripheral skeleton and 60% in the axial skeleton [16]. Positron emission tomography (PET) using 18-fluorodeoxyglucose is increasingly being utilized in the diagnosis of osteomyelitis. In a systematic review and metaanalysis, Termaat et al. found PET scans to have a sensitivity of 96% and a specificity of 91% for the diagnosis of osteomyelitis. [16]. PET scanning is a cheaper modality when compared with other nuclear bone scanning techniques and is typically performed in one day. Unfortunately, however, false positive results can be seen with bone healing. Computed tomography (CT) provides excellent cortical bony details showing cortical bone erosion or destruction and periosteal reaction. It could also show small foci of air within the medullary canal, tiny foreign bodies serving as a nidus for infection and sequestrum formation [17]. Magnetic resonance imaging (MRI) is more sensitive than CT in detecting osteomyelitis and as sensitive as nuclear studies. The sensitivity and specificity of MRI ranged from 82% to 100% and 75% to 96%, respectively. MRI is considered the imaging modality of choice in cases of established osteomyelitis because it allows accurate determination of the extent of the infection, especially in case of vertebral osteomyelitis (identifies epidural abscess, phlegmon, and cord compression) [17]. A.J. EID, E.F. BERBARI Osteomyelitis Lebanese Medical Journal 2012 Volume 60 (1) 53

4 TABLE III ANTIMICROBIAL THERAPY FOR OSTEOMYELITIS DUE TO SPECIFIC MICROORGANISMS Microorganisms First choice Alternative Choice Staphylococci, oxacillin-sensitive Nafcillin sodium or oxacillin sodium, g IV q 4 hr for 4-6 wks Vancomycin*, 20 mg/kg IV q 12 hr for 4-6 wks OR Cefazolin 1-2 g IV q 8 hr for 4-6 wks Staphylococci, oxacillin-resistant Vancomycin*, 15 mg/kg IV q 12 hr for 4-6 wks Linezolid 600 mg PO/IV q 12 hr for 6 wks OR Levofloxacin** mg PO/IV daily and rifampin 600 mg PO daily for 6 wks Penicillin-sensitive streptococci Aqueous crystalline penicillin G, 20 x 10 6 U/24 hr IV, either continuously or Vancomycin*, 20 mg/kg IV q 12 hr for 4-6 wks in 6 equally divided daily doses for 4-6 wks OR Ceftriaxone 1-2 g IV or IM q 24 hr for 4-6 wks OR Cefazolin 1-2 g IV every 8 hr for 4-6 wks Enterococci or streptococci with Aqueous crystalline penicillin G, 20 x 10 6 U/24 hr IV, either continuously or Vancomycin*, 20 mg/kg IV q 12 hr for 4-6 wks penicillin MIC 0.5 µg/ml or in 6 equally divided daily doses for 4-6 wks Optional: Add Gentamicin sulfate, 1 mg/kg IV or IM every 8 hr for 1-2 wks Abiotrophia defectiva, OR Ampicillin sodium 12 g/24 hr IV either continuously or in 6 equally divided Granulicatella spp., Gemella spp. daily doses for 4-6 wks Optional: Add Gentamicin sulfate, 1 mg/kg IV or IM every 8 hr for 1-2 wks Enterobacteriaceae Ceftriaxone 2 g IV q 24 hr for 4-6 wks Ciprofloxacin** mg PO q 24 hr for 4-6 wks Pseudomonas aeruginosa or Cefepime 2 g IV q 12 hr for 4-6 wks Ciprofloxacin** 750 mg PO q 12 hr for 4-6 wks Enterobacter spp. OR Meropenem 1 g IV q 8 hr for 4-6 wks OR Ceftazidime 2 g IV q 8 hr for 4-6 wks hr: hour IM: intramuscular IV: intravenous wks: weeks PO: per os *Dose based on normal creatinine clearance; vancomycin trough level should be **Should be avoided if possible, in the pediatric population and in osteomyelitis associated with fractures. THERAPEUTIC STRATEGIES The optimal treatment of osteomyelitis is still not well defined due to the lack of prospective randomized controlled clinical trials. Most of the data supporting treatment guidelines derive from studies in animal models, expert opinions, and retrospective studies in humans. In general, treatment consists of a combination of surgical debridement and antimicrobial therapy [6]. Both treatment components should be tailored to manage various forms of osteomyelitis. The details of treatment will be discussed in the following sections addressing specific osteomyelitis entities. Medical management In order to establish a microbiological diagnosis and unless the patient is hemodynamically unstable, every effort should be directed at obtaining bone specimens prior to the initiation of empiric antimicrobial therapy. The optimal duration of antimicrobial therapy for osteomyelitis is not known. In an animal model, S. aureus grew from 78% of specimens after 14 days of therapy with clindamycin but only from 16% of specimens after 28 days of therapy. In this model, surgical debridement was not part of the treatment, however [18]. In the clinical setting, relapse is not uncommon even after 4 weeks of antibiotic therapy. Therefore, many experts recommend 4 to 6 weeks of therapy [6]. In some instances, when surgical debridement is suboptimal or lacking, treatment is extended to 8-10 weeks. During treatment, the inflammatory markers (ESR and CRP) are expected to go down when compared to baseline values. In one study of vertebral osteomyelitis, the rate of clinical failure when ESR fell or failed to fall by more than 25% of the baseline value during the first month of treatment was 12% and 50%, respectively [19]. Parenteral antimicrobial therapy is commonly used; however, oral antimicrobials with good bioavailability and bone penetration (e.g. trimethoprim-sulfamethoxazole, clindamycin, tetracyclines, fluoroquinolones, metronidazole, and linezolid) can be used if compliance is ascertained. Betalactams (i.e. intravenous penicillins and cephalosporins) are commonly used to treat osteomyelitis due to their efficacy and relative safety when given for a prolonged period of time [6] (Table III). Vancomycin is used to treat methicillin-resistant S. aureus (MRSA) and ampicillin-resistant Enterococcus species; however, vancomycin use is associated with higher treatment failure rate when compared with betalactams [20]. Data regarding the use of newer drugs such as linezolid and daptomycin for the treatment of osteomyelitis due to MRSA and vancomycin-resistant Enterococcus (VRE) are limited [21-23]. In recent years, osteomyelitis due to resistant Gramnegative bacilli (i.e. multidrug resistant Pseudomonas aeruginosa, extended-spectrum ß-lactamase producing Klebsiella pneumonia and Escherichia coli) has become a serious therapeutic challenge. In those cases, antimicrobial therapy should always be guided by in vitro susceptibility studies. Intravenous colistin and carbapenems (i.e. doripenem) are frequently used and synergy studies could also be considered in difficult cases. The data from animal models suggest that fluoro-

5 quinolones significantly impair fracture healing [24]; therefore, experts recommend caution when using fluoroquinolones for the treatment of osteomyelitis in the context of fractured bone [6]. The use of rifampin for the treatment of staphylococcal osteomyelitis could be beneficial due to biofilm penetration and increased bactericidal activity when co-administered with other antibiotics [25-26], especially in case of hardware-associated osteomyelitis [27-28]. Hyperbaric oxygen therapy (HBOT) can be used in cases of chronic and refractory osteomyelitis but its use remains highly controversial [29]. Surgical treatment The goal of surgery in patients with osteomyelitis is to drain all infected fluid at the site of infection, completely debride all infected and devitalized soft tissue and bone, and achieve good wound coverage. Ideally all infected hardware should be removed; however, this is not possible when the fractured bone is not stable enough. When significant soft tissue defect is present, musculocutaneous flaps can be used to eliminate the dead-space and provide adequate coverage of the wound. Patients presenting with severe and recurrent osteomyelitis might require multiple surgical debridements in order to insure complete removal of the infected tissue. In those situations, antibiotic impregnated polymethyl metacrylate (PMMA) beads can be placed deep into the wound around the infected bone. Those beads allow the local delivery of higher concentrations of antibiotics; however, they should be ultimately removed from the wound. MANAGEMENT OF PATIENTS WITH VARIOUS TYPES OF OSTEOMYELITIS Osteomyelitis in patients with contaminated open fracture Osteomyelitis can develop at the site of an open fracture in 3% to 25% of cases [30-31]. Factors determining the rate of infection include the type of fracture, degree of contamination of the wound (fracture type IIIB), extent of soft tissue injury, the timing of surgical debridement, the use of systemic, and local antimicrobials (i.e. PMMA beads) [30-35]. Patients are usually young men presenting with fractures of the lower extremities, mainly the tibia and fibula. Short course of systemic antibiotic therapy (24 hours) in addition to the use of antibiotic-impregnated PMMA beads is recommended [6] in order to minimize the risk of subsequent osteomyelitis. Antibiotic-impregnated intramedullary nails are being used as well and the preliminary data from retrospective studies showed promise [36-37]. The impact of osteomyelitis in those cases could be devastating due to nonunion of the infected bone and the need for amputation. Patients typically present several months after the accident with nonunion at the fracture site and poor wound healing or draining sinuses. Local signs and systemic symptoms are not common. Imaging studies are not helpful in establishing the diagnosis of osteomyelitis due to bony changes secondary to trauma and surgery and artifacts due to prosthetic material. Following a course of parenteral antimicrobial therapy, oral suppressive therapy should be considered and continued until the fracture heals. In case of relapse of the infection after bone healing, the hardware should be removed and another course of parenteral antimicrobial therapy should be given [6]. Vertebral osteomyelitis and spondylodiskitis Vertebral osteomyelitis and intervertebral disk infection commonly result from hematogenous seeding via the segmental artery supplying two adjacent end plates of contiguous vertebrae [38]. Less frequently, vertebral osteomyelitis and disk space infection complicates spinal surgery. The routine use of preoperative antibiotic prophylaxis further reduced the incidence of postoperative spinal infection. In one study, the rates of infection with and without antimicrobial prophylaxis were 0.2% and 2.8%, respectively [39]. The infection involves most commonly the lumbar spine followed by the thoracic and cervical spine [40-41]. Vertebral osteomyelitis and disk space infection can be complicated with paravertebral and epidural abscesses. The latter could lead to spinal cord or nerve root compression and require urgent surgical intervention. The majority of patients with vertebral osteomyelitis present with back pain while less than half have fever. Neurological symptoms such as motor or sensory deficits, bladder and bowel incontinence are not uncommon and should receive urgent attention. S. aureus is the most commonly isolated organism while coagulase-negative staphylococcus and gram-negative bacilli are less commonly encountered. Pseudomonas aeruginosa and Candida spp. are typically seen in intravenous drug users. Vertebral osteomyelitis due to Brucella spp. and Mycobacterium tuberculosis is common in endemic areas. When bacteremia is present, endocarditis should be ruled out [41-43]. Spine MRI is the test of choice when vertebral osteomyelitis is suspected. Gallium or PET scans are alternatives when MRI cannot be performed (i.e. patients with claustrophobia or patients with implantable cardiovascular devices). If the diagnosis is supported by imaging studies, a microbiological diagnosis should be established. CTguided percutaneous biopsies are easy to perform but have limited sensitivity (52%) [44]. When the results of the first percutaneous biopsy are inconclusive, a second CT-guided biopsy should be attempted before resorting to an open biopsy. Tissue should be submitted for pathology as well as bacterial, fungal and mycobacterial stains and cultures. When the patient has concomitant bacteremia, it is safe to assume that his vertebral osteomyelitis is caused by the same organism isolated from the blood. Surgical debridement is necessary when patients present with an epidural abscess compressing the spinal cord, large paravertebral abscess, spine instability or failing medical treatment [6]. Effective antimicrobial therapy should be given for at least four to six weeks. When vertebral osteomyelitis is treated with surgical debridement and instrumented spine A.J. EID, E.F. BERBARI Osteomyelitis Lebanese Medical Journal 2012 Volume 60 (1) 55

6 fusion or when hardware-associated osteomyelitis develops following spinal surgery, some experts recommend parenteral antibiotic therapy followed by oral suppressive antibiotic therapy for up to two years to allow bone healing [6]. Acute hematogenous osteomyelitis Acute hematogenous osteomyelitis occurs mainly in prepubertal children. Long tubular bones (i.e. femur, tibia, and fibula) are more commonly affected than flat bones and spine [45]. Multiple bones could be infected concomitantly. The infection originates in the metaphyseal region and can extend to the cortex or the epiphysis and joint space. S. aureus and Streptococcus pneumoniae are responsible for most cases. Children present with pain in the metaphyseal region of a long bone. Blood cultures are typically positive. Radiological findings such as periosteal new bone formation (periosteal elevation) or bone destruction support the diagnosis. If plain radiographs are not conclusive, MRI may establish the diagnosis. Blood cultures should be obtained before administering antimicrobials. Bone, subperiosteal exudate, and synovial fluid should be obtained if possible in order to identify the infecting microorganism. Acute hematogenous osteomyelitis in children is frequently treated with antimicrobial therapy alone. Antibiotics are typically given for three weeks. Sequential therapy with intravenous followed by oral antibiotics is commonly used. Surgical treatment is considered in case of no clinical response after 48 hours of antibiotic therapy, septic arthritis, or failure to cure the infection despite adequate antibiotic therapy. Adequate and prompt treatment leads to excellent outcome in newborns, infants and children; however, in cases associated with septic arthritis or complicated with the destruction of the growth plate, the prognosis is more reserved. In those situations, abnormal growth of the affected bone is likely to occur and significant damage of the infected joint might be irreversible [46]. Osteomyelitis in patients with diabetes mellitus Patients with diabetes mellitus are at increased risk of developing foot infections due to hyperglycemia, neuropathy, and peripheral vascular disease. During their lifetime, 15% of diabetic patients develop foot ulcers and 6% are hospitalized because of those ulcers [47]. The infectious process usually originates at the site of an ulcer and commonly progresses to reach contiguous bone. When the size of an ulcer is > 2 x 2 cm and when ESR is > 70 mm/hour, osteomyelitis is more likely to be present [48]. The presence of exposed bone or the ability to probe the bone is strongly suggestive of underlying osteomyelitis (positive predictive value of 89%) [9, 48-49]. Further testing is not required when the probe-to-bone test is positive. In other situations, plain radiographs, nuclear bone scans, or MRI could be helpful to establish the diagnosis. ESR and CRP should always be measured at baseline and monitored during therapy to assess response. Chronic osteomyelitis in patients with diabetes mellitus is usually polymicrobial. Multiple aerobic and anaerobic bacteria can be involved. When possible, bone tissue should be submitted for cultures prior to the initiation of antimicrobial therapy. When hemodynamically significant stenosis is present, revascularization should be considered before surgical debridement of the infected foot. Intravenous antimicrobials such as piperacillin-tazobactam, ticarcillin-clavulanate, ampicillin-sulbactam, Ertapenem, or other ß-lactams in combination with metronidazole are commonly used. An oral regimen consisting of levofloxacin or moxifloxacin with metronidazole or clindamycin can also be used [50]. HBOT might be beneficial in this context due to limited oxygenation of the infected tissue and the likelihood of anaerobic infection; however, data from randomized, controlled studies are lacking. Limited amputation of the limb should be considered in cases with persistent or recurrent osteomyelitis despite optimal therapy. Osteomyelitis associated with prosthetic joint infection Joint arthroplasty represent a true success story due to its ability to restore function. The projected number of patients who will undergo arthroplasty in the United States in 2030 is 3-4 millions [51]. It is estimated that 0.8 to 1.9% of knee arthroplasties and 0.3 to 1.7% of hip arthroplasties get infected [52]. The treatment also consists of a combination of surgical and antimicrobial therapy. Three different therapeutic strategies are available: 1. Surgical debridement and retention of the prosthesis is an option when certain criteria are met. Those include duration of symptoms < 3 weeks, infection developing within 3 months of arthroplasty or presentation consistent with hematogenous seeding, well-fixed prosthesis, adequate soft tissue envelop, absence of sinus tract, and established microbiologic diagnosis and favorable susceptibility profile [52-53]. 2. One-stage exchange entails resection of the infected prosthesis, debridement of the infected tissue and immediate implantation of a new prosthesis. Antibioticimpregnated PMMA cement is frequently used during reimplantation. This strategy is not advisable when the infection is caused by virulent organisms (i.e. S. aureus, Gram-negative bacteria) or in presence of draining sinus or significant purulence. 3. Two-stage exchange consists of resection of the infected prosthesis followed by parenteral antimicrobial therapy for 4-6 weeks and reimplantation of a new prosthesis 2-6 weeks after finishing antimicrobial therapy. The use of a spacer impregnated with antimicrobial(s) (i.e. vancomycin, gentamicin or tobramycin) is a common practice currently and was shown to reduce the rate of recurrent infection [54]. Antimicrobial therapy should be guided by in vitro susceptibilities (Table III). Following debridement and retention of the prosthesis, Rifampin was successfully used in combination with fluoroquinolones. The duration of treatment was 3-6 months for prosthetic knee infection and 6 months for prosthetic hip infection [27, 55]. Shorter 56 Lebanese Medical Journal 2012 Volume 60 (1) A.J. EID, E.F. BERBARI Osteomyelitis

7 course (4 weeks) of parenteral antibiotic therapy can be given followed by suppressive oral antibiotic therapy [56]. Rifampin-based regimen is also recommended after onestage exchange. Osteomyelitis in injection drug users Intravenous drug use is associated with hematogenous osteomyelitis due to the introduction of bacteria and fungi into the bloodstream. However, direct inoculation or contiguous spread is also possible [6]. Multifocal infections may occur. The spine, sterno-clavicular, sterno-chondral, and sacro-iliac joints are commonly involved [57-58]. The most common organisms responsible for osteomyelitis in injection drug users (IDU) are S. aureus, Pseudomonas species, and Candida species. Eikenella corrodens, which is part of the normal oral flora, is seen in IDU who lick their needles or skin prior to injection ( needle licker s osteomyelitis ) [59]. M. tuberculosis can cause skeletal infection in IDU and most cases involve the spine [60]. Treatment of osteomyelitis in IDU is similar to treatment of other patients; however, an oral regimen should be used, if at all possible, to avoid using long-term intravenous access (e.g. peripherally inserted intravenous catheter). Osteomyelitis due to Brucella species Brucellosis is endemic in the Mediterranean basin and the Arabian Gulf; therefore, osteomyelitis due to Brucella species should be considered in this setting. Brucellosis is commonly transmitted via ingestion of contaminated food such as raw milk, cheese made from unpasteurized milk, or raw meat. Infection could also result from direct skin inoculation through skin abrasions or cuts during contact with animal carcasses, placentas, and animal vaginal secretions. Patients present with fever, night sweats, arthralgias, anorexia and fatigue. When the diagnosis is delayed, localized infection occurs. Osteoarticular infections, mainly sacroiliitis, represent 20-30% of those localized infections [61-62]. Specific cultures (Ruiz-Castaneda or lysis centrifugation) or prolonged incubation of cultures can be used to establish a diagnosis. Serological studies using serum agglutination (standard tube agglutination) and enzyme-linked immunosorbent assay (ELISA) can be very helpful, especially in case of negative cultures. The combination of doxycycline-streptomycin or doxycyclinestreptomycin-rifampin seem to be more effective than doxycycline-rifampim [63-64]. Ciprofloxacin-rifampin can be considered as an alternative regimen for doxycycline-streptomycin when patients experience drug toxicity [65]. Osteoarticular disease, similar to other localizing manifestations, carries with it higher risk of relapse compared to brucellosis without localizing disease. Therefore, antibiotic therapy should be administered for 3-6 months [61, 64] in order to minimize the risk of relapse. Osteomyelitis due to Salmonella species Osteomyelitis due to Salmonella species is uncommon accounting for 0.45% of all osteomyelitis cases and is seen in only 0.8% of all Salmonella infections [66]. Patients with sickle cell disease, however, have much higher risk of developing this infection. Other risk factors include comorbidities such as diabetes mellitus, systemic lupus erythematosus, lymphoma, liver disease, previous surgery or trauma, treatment with steroids, and extremes of age [66]. Patients are usually treated with third-generation cephalosporins or fluoroquinolones. In anecdotal reports, the duration of successful antibiotic therapy ranged from 6-12 weeks [66-69]. Osteomyelitis due to mycobacteria Osteomyelitis can result from infection due to M. tuberculosis or non-tuberculous mycobacteria (NTBM). Mycobacterial osteomyelitis should be suspected when bacterial cultures remain negative or when granulomatous inflammation is identified in bone tissue [70]. Tuberculosis (TB) of the musculoskeletal system represents 1-5% of all TB cases [6]. Osteomyelitis is attributed to hematogenous seeding of the bone at the time of primary infection and should be considered in patients with history of treated or untreated tuberculosis, known exposure to M. tuberculosis, positive tuberculin skin test, and evidence of old or active TB on chest X-ray. Pott s disease or vertebral osteomyelitis due to M. tuberculosis represents around 50% of all musculoskeletal TB cases [71]. The lumbar and lower thoracic spine is more commonly involved than the upper thoracic and cervical spine [72-73]. In 50% of cases, spine MRI shows evidence of paravertebral abscesses and those are frequently bilateral. Extraspinal tuberculosis presents with swelling, pain, and mild erythema. A cold abscess is usually present and spontaneous drainage through a sinus tract could occur. The most common manifestations of spinal osteomyelitis are pain and stiffness. Due to delayed diagnosis, neurological deficit due to spinal cord compression is present in 42-76% of patients [74-75]. Treatment of tuberculous osteomyelitis is for the most part medical. The regimens of antituberculous medications used to treat osteoarticular TB are similar to those used to treat other forms of TB, but treatment should be given for a longer period of time (12-18 months) [76]. Surgical therapy might be necessary for abscess drainage, cord decompression, and spinal stabilization [74]. Musculoskeletal infections due to NTBM seem to have increased in frequency over the past few years, possibly due to better recognition of this infection [77]. Multiple species can be responsible for osteomyelitis and those include M. abscessus, M. chelonae, M. fortuitum, M. marinum, M. avium-intracellulare, M. kansasii, M. xenopi and M. terrae complex [78-81]. The infection develops in bones, joints, bursae, or tendon sheaths following direct inoculation at the time of surgery, trauma, puncture wounds, or injections (intraarticular or extraarticular). Patients present with non-healing wounds associated with chronic drainage and sinus formation. Axial bone or extremities could also be infected through hematogenous seeding. Mycobacterial cultures of tissue specimens are required to establish a diagnosis; however, rapidly-grow- A.J. EID, E.F. BERBARI Osteomyelitis Lebanese Medical Journal 2012 Volume 60 (1) 57

8 ing mycobacteria grow on routine cultures as well. The identification of the infecting species and its susceptibility profile are crucial to guide antimicrobial therapy. A combination of two or three antibiotics (depending upon the degree of severity of the infection) should be used to treat the infection. The antibiotics should be determined based on the susceptibility profile. Osteomyelitis due to rapidlygrowing mycobacteria is treated for six months while osteomyelitis due to other mycobacteria is treated for at least 12 months [82]. Osteomyelitis due to fungi Fungal osteomyelitis is more likely to result from disseminated fungal infection than direct inoculation of the bone. Osteomyelitis is commonly seen with disseminated endemic fungal infections such as blastomycosis, coccidioidomycosis and sporotrichosis. Up to 25% of patients with disseminated blastomycosis develop osteomyelitis [83]. Candida osteomyelitis can complicate candidemia or result from surgical site infection. Even though uncommon, disseminated Aspergillus and Cryptococcus infections in immunocompromised patients can lead to osteomyelitis. Fungal osteomyelitis due to molds such as Pseudollascheria boydii, Scedosporium prolificans, and Fusarium species is usually seen with open contaminated fractures. The clinical context is often helpful to identify the fungus responsible for osteomyelitis. The role of surgical treatment is relatively limited and the medical treatment depends on the etiology. Recurrent osteomyelitis Patients presenting with recurrent osteomyelitis should undergo comprehensive evaluation in order to determine the underlying etiology. Recurrence of osteomyelitis could be attributed to a variety of factors. Those include incorrect microbiological diagnosis, inability to culture the true pathogen (e.g. Mycobacteria, Coxiella, Mycoplasma, and Chlamydia species), use of inappropriate or suboptimal dose of antimicrobial(s), development of resistance of the infecting organism, and inadequate surgical debridement of the infected bone. Occasionally, failure of treatment is attributed solely to the virulence of the infecting bacteria (e.g. Brucella species, MRSA). Antibiotic therapy should be held for at least two weeks prior to repeat surgical debridement. Tissue specimens must be submitted for aerobic and anaerobic bacterial, as well as fungal and mycobacterial cultures. Following surgery, antimicrobial therapy should be guided by culture results and in vitro susceptibilities. CONCLUSION Osteomyelitis continues to be a serious infection associated with high relapse rate and significant morbidity and loss of function. Preventive strategies should be emphasized and widely implemented in order to reduce the incidence, especially in high risk patients such as those with diabetes mellitus. When osteomyelitis develops, the patient should be treated by a multidisciplinary team including an orthopedic surgeon, vascular surgeon, plastic surgeon, interventional radiologist, endocrinologist and an infectious diseases specialist. Such an approach provides the best chance for cure and restoration of function. REFERENCES 1. Belmatoug N, Cremieux AC, Bleton R et al. A new model of experimental prosthetic joint infection due to methicillin-resistant Staphylococcus aureus : a microbiologic, histopathologic, and magnetic resonance imaging characterization. J Infect Dis 1996 Aug ; 174 (2) : Lew DP, Waldvogel FA. Osteomyelitis. N Engl J Med 1997 Apr 3 ; 336 (14) : Norden CW. Lessons learned from animal models of osteomyelitis. Rev Infect Dis 1988 Jan-Feb ; 10 (1) : Ciampolini J, Harding KG. Pathophysiology of chronic bacterial osteomyelitis. Why do antibiotics fail so often? Postgrad Med J 2000 Aug ; 76 (898) : Muller C, Zielinski CC, Passl R, Eibl MM. Divergent patterns of leucocyte locomotion in experimental posttraumatic osteomyelitis. Br J Exp Pathol 1984 Jun ; 65 (3) : Berbari EF, Steckelberg JM, Osmon DR. Osteomyelitis. In : Mandell, Douglas and Bennett s Principles and Practice of Infectious Diseases, 7 th edition, Volume 1. Edinburgh, UK : Churchill Livingstone, Chihara S, Segreti J. Osteomyelitis. Dis Mon 2010 Jan ; 56 (1) : Mader JT, Shirtliff M, Calhoun JH. Staging and staging application in osteomyelitis. Clin Infect Dis 1997 Dec ; 25 (6) : 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 Mar 1 ; 273 (9) : Perry CR, Pearson RL, Miller GA. Accuracy of cultures of material from swabbing of the superficial aspect of the wound and needle biopsy in the preoperative assessment of osteomyelitis. J Bone Joint Surg Am 1991 Jun ; 73 (5) : Mackowiak PA, Jones SR, Smith JW. Diagnostic value of sinus-tract cultures in chronic osteomyelitis. JAMA 1978 Jun 30 ; 239 (26) : Dinh MT, Abad CL, Safdar N. Diagnostic accuracy of the physical examination and imaging tests for osteomyelitis underlying diabetic foot ulcers : meta-analysis. Clin Infect Dis 2008 Aug 15 ; 47 (4) : Schauwecker DS. The scintigraphic diagnosis of osteomyelitis. Am J Roentgenol 1992 Jan ; 158 (1) : Gotthardt M, Bleeker-Rovers CP, Boerman OC, Oyen WJ. Imaging of inflammation by PET, conventional scintigraphy, and other imaging techniques. J Nucl Med Dec ; 51 (12) : Hadjipavlou AG, Cesani-Vazquez F, Villaneuva-Meyer J, et al. The effectiveness of gallium citrate Ga 67 radionuclide imaging in vertebral osteomyelitis revisited. 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9 tematic review and meta-analysis. J Bone Joint Surg Am 2005 Nov ; 87 (11) : Pineda C, Vargas A, Rodriguez AV. Imaging of osteomyelitis : current concepts. Infect Dis Clin North Am 2006 Dec ; 20 (4) : Norden CW, Shinners E, Niederriter K. Clindamycin treatment of experimental chronic osteomyelitis due to Staphylococcus aureus. J Infect Dis 1986 May ; 153 (5) : Carragee EJ, Kim D, van der Vlugt T, Vittum D. The clinical use of erythrocyte sedimentation rate in pyogenic vertebral osteomyelitis. Spine (Phila Pa 1976) 1997 Sep 15 ; 22 (18) : Tice AD, Hoaglund PA, Shoultz DA. Outcomes of osteomyelitis among patients treated with outpatient parenteral antimicrobial therapy. Am J Med 2003 Jun 15 ; 114 (9) : Razonable RR, Osmon DR, Steckelberg JM. Linezolid therapy for orthopedic infections. Mayo Clin Proc 2004 Sep ; 79 (9) : Rao N, Hamilton CW. Efficacy and safety of linezolid for Gram-positive orthopedic infections : a prospective case series. Diagn Microbiol Infect Dis 2007 Oct ; 59 (2) : Rao N, Regalla DM. Uncertain efficacy of daptomycin for prosthetic joint infections : a prospective case series. Clin Orthop Relat Res 2006 Oct ; 451 : Huddleston PM, Steckelberg JM, Hanssen AD, Rouse MS, Bolander ME, Patel R. Ciprofloxacin inhibition of experimental fracture healing. J Bone Joint Surg Am 2000 Feb ; 82 (2) : Norden CW. Experimental chronic staphylococcal osteomyelitis in rabbits : treatment with rifampin alone and in combination with other antimicrobial agents. Rev Infect Dis 1983 Jul-Aug ; 5 (Suppl 3) : S491-S Shirtliff ME, Mader JT, Calhoun J. Oral rifampin plus azithromycin or clarithromycin to treat osteomyelitis in rabbits. Clin Orthop Relat Res 1999 Feb (359) : Zimmerli W, Widmer AF, Blatter M, Frei R, Ochsner PE. Role of rifampin for treatment of orthopedic implantrelated staphylococcal infections : a randomized controlled trial. Foreign-Body Infection (FBI) Study Group. JAMA 1998 May 20 ; 279 (19) : Perlroth J, Kuo M, Tan J, Bayer AS, Miller LG. Adjunctive use of rifampin for the treatment of Staphylococcus aureus infections : a systematic review of the literature. Arch Intern Med 2008 Apr 28 ; 168 (8) : Kranke P, Bennett M, Roeckl-Wiedmann I, Debus S. Hyperbaric oxygen therapy for chronic wounds. Cochrane Database Syst Rev 2004 (2) : CD Ostermann PA, Seligson D, Henry SL. Local antibiotic therapy for severe open fractures. A review of 1085 consecutive cases. J Bone Joint Surg Br 1995 Jan ; 77 (1) : Sterett WI, Ertl JP, Chapman MW, Moehring HD. Open tibia fractures in the splenectomized trauma patient : results of treatment with locking, intramedullary fixation. J Trauma 1995 Apr ; 38 (4) : DeLong WG Jr., Born CT, Wei SY, Petrik ME, Ponzio R, Schwab CW. Aggressive treatment of 119 open fracture wounds. J Trauma 1999 Jun ; 46 (6) : Holcombe SJ, Schneider RK, Bramlage LR, Embertson RM. Use of antibiotic-impregnated polymethyl methacrylate in horses with open or infected fractures or joints : 19 cases ( ). J Am Vet Med Assoc 1997 Oct 1 ; 211 (7) : Henry SL, Ostermann PA, Seligson D. The prophylactic use of antibiotic impregnated beads in open fractures. J Trauma 1990 Oct ; 30 (10) : Kindsfater K, Jonassen EA. Osteomyelitis in grade II and III open tibia fractures with late debridement. J Orthop Trauma 1995 Apr ; 9 (2) : Shyam AK, Sancheti PK, Patel SK, Rocha S, Pradhan C, Patil A. Use of antibiotic cement-impregnated intramedullary nail in treatment of infected non-union of long bones. Indian J Orthop 2009 Oct ; 43 (4) : Qiang Z, Jun PZ, Jie XJ, Hang L, Bing LJ, Cai LF. Use of antibiotic cement rod to treat intramedullary infection after nailing : preliminary study in 19 patients. Arch Orthop Trauma Surg 2007 Dec ; 127 (10) : Wiley AM, Trueta J. The vascular anatomy of the spine and its relationship to pyogenic vertebral osteomyelitis. J Bone Joint Surg Br 1959 Nov ; 41-B : Schnoring M, Brock M. [Prophylactic antibiotics in lumbar disc surgery : analysis of 1,030 procedures]. Zentralbl Neurochir 2003 ; 64 (1) : Torda AJ, Gottlieb T, Bradbury R. Pyogenic vertebral osteomyelitis : analysis of 20 cases and review. Clin Infect Dis 1995 Feb ; 20 (2) : Hopkinson N, Stevenson J, Benjamin S. A case ascertainment study of septic discitis : clinical, microbiological and radiological features. QJM 2001 Sep ; 94 (9) : Pigrau C, Almirante B, Flores X et al. Spontaneous pyogenic vertebral osteomyelitis and endocarditis : incidence, risk factors, and outcome. Am J Med 2005 Nov ; 118 (11) : Vlahakis NE, Temesgen Z, Berbari EF, Steckelberg JM. Osteoarticular infection complicating enterococcal endocarditis. Mayo Clin Proc 2003 May ; 78 (5) : Nolla JM, Ariza J, Gomez-Vaquero C et al. Spontaneous pyogenic vertebral osteomyelitis in nondrug users. Semin Arthritis Rheum 2002 Feb ; 31 (4) : Vazquez M. Osteomyelitis in children. Curr Opin Pediatr 2002 Feb ; 14 (1) : De Boeck H. Osteomyelitis and septic arthritis in children. Acta Orthop Belg 2005 Oct ; 71 (5) : Ramsey SD, Newton K, Blough D et al. Incidence, outcomes, and cost of foot ulcers in patients with diabetes. Diabetes Care 1999 Mar ; 22 (3) : Butalia S, Palda VA, Sargeant RJ, Detsky AS, Mourad O. Does this patient with diabetes have osteomyelitis of the lower extremity? JAMA 2008 Feb 20 ; 299 (7) : Newman LG, Waller J, Palestro CJ et al. Unsuspected osteomyelitis in diabetic foot ulcers. Diagnosis and monitoring by leukocyte scanning with indium in 111 oxyquinoline. JAMA 1991 Sep 4 ; 266 (9) : Lipsky BA, Berendt AR, Deery HG et al. Diagnosis and treatment of diabetic foot infections. Clin Infect Dis 2004 Oct 1 ; 39 (7) : Kurtz S, Ong K, Lau E, Mowat F, Halpern M. Projections of primary and revision hip and knee arthroplasty in the United States from 2005 to J Bone Joint Surg Am 2007 Apr ; 89 (4) : Del Pozo JL, Patel R. Clinical practice. Infection associated with prosthetic joints. N Engl J Med 2009 Aug 20 ; 361 (8) : Brause B. Infections with prostheses in bones and joints. A.J. EID, E.F. BERBARI Osteomyelitis Lebanese Medical Journal 2012 Volume 60 (1) 59

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