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Pathophysiology of Chronic Bacterial Osteomyelitis. Why Do Antibiotics Fail Postgrad Med J 2000;76:479–483 479 Pathophysiology of chronic bacterial osteomyelitis. Postgrad Med J: first published as 10.1136/pmj.76.898.479 on 1 August 2000. Downloaded from Why do antibiotics fail so often? J Ciampolini, K G Harding Abstract sinuses overlying a focus of chronic osteomyeli- In this review the pathophysiology of tis. Mackowiack in 1978 demonstrated the low chronic bacterial osteomyelitis is summa- positive predictive value of sinus tract swabs; in rised, focusing on how bacteria succeed so a retrospective analysis of 40 patients, only often in overcoming both host defence 44% of the soft tissue swabs contained the mechanisms and antibiotic agents. Bacte- same pathogen as that obtained from a bone ria adhere to bone matrix and orthopae- sample at the time of operation. However, iso- dic implants via receptors to fibronectin lation of Staphylococcus aureus from the sinus and to other structural proteins. They tract swab had a higher positive predictive subsequently elude host defences and value than for other bacteria (78%). The same antibiotics by “hiding” intracellularly, by study found 60% of chronic osteomyelitis to be developing a slimy coat, or by acquiring a due to S aureus, followed by enterobacteriaceae very slow metabolic rate. The presence of (23%), pseudomonas (9%) and streptococcus an orthopaedic implant also causes a local (9%).3 Similar results with regards to the inac- polymorphonuclear cell defect, with de- curacy of wound swabs were obtained in creased ability to kill phagocytosed bacte- prospective studies on diabetic foot infection4 ria. Osteolysis is determined locally by the and on post-traumatic chronic osteomyelitis.5 interaction of bacterial surface compo- The latter study also demonstrated the poor nents with immune system cells and positive predictive value of Craig needle biopsy subsequent cytokine production. The in- specimens. Accurate identification of the creasing development of antibiotic resist- micro-organism and its sensitivity can there- ance by Staphylococcus aureus and S fore only be obtained by an open surgical pro- epidermidis will probably make conserva- cedure, and there appears little (if any at all) tive treatment even less successful than it place for non-invasive diagnostic methods. is now. A close interaction between ortho- From cultures of operative specimens, S paedic surgeons and physicians, with aureus is the main causative agent of chronic combined medical and operative treat- bacterial osteomyelitis, accounting for about two ment, is to be commended. thirds of the isolates, followed by pseudomonas (Postgrad Med J 2000;76:479–483) and enterobacteriaceae.356 Osteomyelitis com- http://pmj.bmj.com/ Keywords: osteomyelitis; joint replacement infection; plicating diabetic foot infection, however, is antibiotics; osteolysis typically polymicrobial, with mixed aerobes, fac- ultative anaerobes, and strict anaerobes being isolated at operation.4 Coagulase negative Sta- Acute bacterial osteomyelitis carried a 50% phylococcus spp, such as S epidermidis, are mortality in the preantibiotic era because of responsible for the majority of chronic osteomy- overwhelming sepsis with metastatic 1 elitis associated with orthopaedic implants and abscesses. Although antimicrobial drugs have 78 for 90% of pin tract infections. Other less on September 26, 2021 by guest. Protected copyright. dramatically changed the prognosis of the common micro-organisms isolated include sal- acute haematogenous form, chronic bacterial monella (more frequent in developing coun- osteomyelitis remains a challenging medical tries), and anaerobes such as clostridium and problem. Despite advances in antibiotic devel- 469 Pasteurella multocida. opment, it all too often remains refractory to Box 1 summarises the above section. chemotherapeutic treatment alone.2 The rapid development of antibiotic resistance by Staphy- lococcus spp will probably demand more frequently a strategy of combined medical and Box 1: Micro-organisms surgical treatment in the near future. x The typical causative agent is S aureus, Wound Healing In this review we analyse the current under- Research Unit, or S epidermidis if associated with an standing of chronic osteomyelitis by focusing implant. Gram negative bacteria are University of Wales on how bacteria succeed in overcoming both College of Medicine, present in about one third of cases. CardiV,UK host defence mechanisms and the antibiotic J Ciampolini agents. x Chronic osteomyelitis in the diabetic K G Harding foot is polymicrobial with mixed Gram Discharging sinus and the underlying positive and Gram negative bacteria Correspondence to: (aerobes and anaerobes). Mr J Ciampolini, Princess bone: micro-organisms involved Elizabeth Orthopaedic A clinician treating a patient with a suspected x Wound swabs are all too often inaccurate Centre, Exeter, Devon EX2 infected wound will usually send a superficial in chronic osteomyelitis: cultures from 5DW, UK pus swab to the laboratory and institute operative specimens are a more reliable Submitted 19 March 1999 antibiotic therapy accordingly. Particular prob- method of planning antibiotic treatment. Accepted 5 July 1999 lems, however, exist for wounds that are in fact www.postgradmedj.com 480 Ciampolini, Harding Postgrad Med J: first published as 10.1136/pmj.76.898.479 on 1 August 2000. Downloaded from Pathophysiology of bone infection Infection Rodet produced the first experimental acute haematogenous osteomyelitis in 1884: injec- tion of rabbits with “un micrococcus qu’il pos- Local factors General factors sede une couleur jaune orange” (S aureus) resulted in the occurrence of multiple bone • Presence of foreign body • Diabetes abscesses.10 Since then various animal models • Bone necrosis • Peripheral vascular • Heavy contamination disease have been studied, including rodents, chicks, • Obesity, smoking, etc rabbits, dogs11 and, more recently, sheep.12 The development and progression of the disease • Bacteria: slow metabolic can be summarised in bacterial contamination rate and adhesion followed by infection and subse- • Covered in slime quent chronicity. Patient predisposing factors • Hide intracellularly intervene at various levels (fig 1). • Host defence defect caused by implant • Osteolysis PATIENT PREDISPOSING FACTORS Healthy bone tissue is extremely resistant to infection.13 14 The presence of bone necrosis, Chronicity heavy contamination or foreign bodies, as well Figure 2 Pathogenetic factors behind the chronicity of a as general predisposing factors such as diabetes bone infection. and peripheral vascular disease tip the balance example, trauma or surgery, or by direct spread in favour of the bacterium. from an adjacent soft tissue infection (for Trauma or surgery can produce devitalised example diabetic foot ulcer or periodontal dis- bone fragments. The other single most potent ease). Whatever the route of access, bacteria bone necrotising factor is indeed ischaemia. In must be able to subsequently adhere to the chick model of haematogenous osteomyeli- components of the bone matrix in order to start tis, patchy ischaemic bone necrosis occurs the infection. when the infective process occludes the vascu- S aureus has been known to bind fibrinogen lar tunnels. This creates an ideal culture for some decades. This may well provide an medium for bacteria, and at 48 hours, explanation for the ability of this micro- abscesses are formed. A sequestrum develops organism to survive in body fluids. Bacteria within eight days.15 clump together and are covered in a layer of The role of bone necrosis is pivotal to the fibrinogen, thus protected from host defence establishment of experimental chronic osteo- mechanisms and antibiotics.17 However, this myelitis by direct inoculum: Norden and alone does not explain how bacteria adhere to Kennedy in 1970 used intramedullary sodium bone matrix. Staphylococcus spp express high morrhuate, a sclerosing agent, before direct aYnity receptors (adhesins) for fibronectin,18 19 inoculation of S aureus in order to obtain collagen,20 and laminin.21 osteomyelitis in rabbits. Inoculation of bacteria Fibronectin, a glycoprotein found in many without sodium morrhuate or vice versa failed body fluids and connective tissue matrices, http://pmj.bmj.com/ to produce an infection.16 appears to be particularly relevant to the pathogenesis of chronic osteomyelitis: bacterial BACTERIAL CONTAMINATION AND ADHESION. adherence to polymers similar to the ones used DEVELOPMENT OF INFECTION in orthopaedic surgery is mediated by Bacteria may reach the bone via the blood- fibronectin.22 23 Fibronectin, fibrinogen, and stream, by direct inoculum caused by, for laminin have been demonstrated to be respon- sible for adherence of S aureus to the surface of on September 26, 2021 by guest. Protected copyright. Bacterial contamination a foreign body in an animal model.24 The same (direct inoculus, intraoperative glycoprotein has been shown to mediate bacte- contamination, haematogenous) rial adhesion to metal plates and screws.25 Sublethal doses of antibiotics have been shown to inhibit mucosal adhesion by group A streptococci and Escherichia coli.26 This is an interesting finding that may provide part of the biological explanation for the eYcacy of Bacterial adhesion prophylactic intravenous antibiotics in ortho- to bone or implant paedic surgery. CHRONICITY ASSOCIATED WITH AN IMPLANT Persistence of bone infection will result in chronic osteomyelitis. The main factors re- Patient predisposing sponsible for the development of chronicity are
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