Abstract
Musculoskeletal infections caused by Staphylococcus aureus are among the most difficult-to-treat infections. S. aureus osteomyelitis is associated with a tremendous disease burden through potential for long-term relapses and functional deficits. Although considerable advances have been achieved in diagnosis and treatment of osteomyelitis, the management remains challenging and impact on quality of life is still enormous. S. aureus acute arthritis is relatively seldom in general population, but the incidence is considerably higher in patients with predisposing conditions, particularly those with rheumatoid arthritis. Rapidly destructive course with high mortality and disability rates makes urgent diagnosis and treatment of acute arthritis essential. S. aureus pyomyositis is a common disease in tropical countries, but it is very seldom in temperate regions. Nevertheless, the cases have been increasingly reported also in non-tropical countries, and the physicians should be able to timely recognize this uncommon condition and initiate appropriate treatment. The optimal management of S. aureus-associated musculoskeletal infections requires a strong interdisciplinary collaboration between all involved specialists.
References
Agarwal JP, Ogilvie M, Wu LC, Lohman RF, Gottlieb LJ, Franczyk M, Song DH (2005) Vacuum-assisted closure for sternal wounds: a first-line therapeutic management approach. Plast Reconstr Surg 116:1035–1040
Anguita-Alonso P, Hanssen AD, Osmon DR, Trampuz A, Steckelberg JM, Patel R (2005) High rate of aminoglycoside resistance among staphylococci causing prosthetic joint infection. Clin Orthop Relat Res 439:43–47
Antunes PE, Bernardo JE, Eugenio L, de Oliveira JF, Antunes MJ (1997) Mediastinitis after aorto-coronary bypass surgery. Eur J Cardiothorac Surg 12:443–449
Aytaç S, Schnetzke M, Swartman B, Herrmann P, Woelfl C, Heppert V, Gruetzner PA, Guehring T (2014) Posttraumatic and postoperative osteomyelitis: surgical revision strategy with persisting fistula. Arch Orthop Trauma Surg 134:159–165
Babouee Flury B, Elzi L, Kolbe M, Frei R, Weisser M, Scharen S, Widmer AF, Battegay M (2014) Is switching to an oral antibiotic regimen safe after 2 weeks of intravenous treatment for primary bacterial vertebral osteomyelitis? BMC Infect Dis 14:226
Barrington NA (1988) The radiology of bone and joint infection. Br J Hosp Med 40:464–472
Becker K, Heilmann C, Peters G (2014) Coagulase-negative staphylococci. Clin Microbiol Rev 27:870–926
Berbari EF, Kanj SS, Kowalski TJ, Darouiche RO, Widmer AF, Schmitt SK, Hendershot EF, Holtom PD, Huddleston PM III, Petermann GW, Osmon DR (2015) 2015 Infectious Diseases Society of America (IDSA) clinical practice guidelines for the diagnosis and treatment of native vertebral osteomyelitis in adults. Clin Infect Dis 61:e26–e46
Bernard A, Kermarrec G, Parize P, Caruba T, Bouvet A, Mainardi JL, Sabatier B, Nich C (2015a) Dramatic reduction of clindamycin serum concentration in staphylococcal osteoarticular infection patients treated with the oral clindamycin-rifampicin combination. J Infect 71:200–206
Bernard L, Dinh A, Ghout I, Simo D, Zeller V, Issartel B, Le M, V, Belmatoug N, Lesprit P, Bru JP, Therby A, Bouhour D, Denes E, Debard A, Chirouze C, Fevre K, Dupon M, Aegerter P, Mulleman D (2015b) Antibiotic treatment for 6 weeks versus 12 weeks in patients with pyogenic vertebral osteomyelitis: an open-label, non-inferiority, randomised, controlled trial. Lancet 385:875–882
Bickels J, Ben-Sira L, Kessler A, Wientroub S (2002) Primary pyomyositis. J Bone Joint Surg Am 84-A:2277–2286
Bischoff M, Dunman P, Kormanec J, Macapagal D, Murphy E, Mounts W, Berger-Bachi B, Projan S (2004) Microarray-based analysis of the Staphylococcus aureus sigmaB regulon. J Bacteriol 186:4085–4099
Blyth MJ, Kincaid R, Craigen MA, Bennet GC (2001) The changing epidemiology of acute and subacute haematogenous osteomyelitis in children. J Bone Joint Surg Br 83:99–102
Boody BS, Jenkins TJ, Maslak J, Hsu WK, Patel AA (2015) Vertebral osteomyelitis and spinal epidural abscess: an evidence-based review. J Spinal Disord Tech 28:E316–E327
Borger MA, Rao V, Weisel RD, Ivanov J, Cohen G, Scully HE, David TE (1998) Deep sternal wound infection: risk factors and outcomes. Ann Thorac Surg 65:1050–1056
Breusch SJ, Kuhn KD (2003) Bone cements based on polymethylmethacrylate. Orthopade 32:41–50
Buchholz HW, Elson RA, Engelbrecht E, Lodenkamper H, Rottger J, Siegel A (1981) Management of deep infection of total hip replacement. J Bone Joint Surg Br 63-B:342–353
Campoccia D, Speziale P, Ravaioli S, Cangini I, Rindi S, Pirini V, Montanaro L, Arciola CR (2009) The presence of both bone sialoprotein-binding protein gene and collagen adhesin gene as a typical virulence trait of the major epidemic cluster in isolates from orthopedic implant infections. Biomaterials 30:6621–6628
Caputo GM, Cavanagh PR, Ulbrecht JS, Gibbons GW, Karchmer AW (1994) Assessment and management of foot disease in patients with diabetes. N Engl J Med 331:854–860
Carragee EJ (1997) The clinical use of magnetic resonance imaging in pyogenic vertebral osteomyelitis. Spine (Phila Pa 1976) 22:780–785
Carragee EJ, Kim D, van der Vlugt T, Vittum D (1997) The clinical use of erythrocyte sedimentation rate in pyogenic vertebral osteomyelitis. Spine (Phila Pa 1976) 22:2089–2093
Ceroni D, Cherkaoui A, Ferey S, Kaelin A, Schrenzel J (2010) Kingella kingae osteoarticular infections in young children: clinical features and contribution of a new specific real-time PCR assay to the diagnosis. J Pediatr Orthop 30:301–304
Chauhan S, Jain S, Varma S, Chauhan SS (2004) Tropical pyomyositis (myositis tropicans): current perspective. Postgrad Med J 80:267–270
Chiedozi LC (1979) Pyomyositis. Review of 205 cases in 112 patients. Am J Surg 137:255–259
Christin L, Sarosi GA (1992) Pyomyositis in North America: case reports and review. Clin Infect Dis 15:668–677
Ciampolini J, Harding KG (2000) Pathophysiology of chronic bacterial osteomyelitis. Why do antibiotics fail so often? Postgrad Med J 76:479–483
Clarke SR, Foster SJ (2006) Surface adhesins of Staphylococcus aureus. Adv Microb Physiol 51:187–224
Clerc O, Prod’hom G, Greub G, Zanetti G, Senn L (2011) Adult native septic arthritis: a review of 10 years of experience and lessons for empirical antibiotic therapy. J Antimicrob Chemother 66:1168–1173
Coakley G, Mathews C, Field M, Jones A, Kingsley G, Walker D, Phillips M, Bradish C, McLachlan A, Mohammed R, Weston V (2006) BSR & BHPR, BOA, RCGP and BSAC guidelines for management of the hot swollen joint in adults. Rheumatology (Oxford) 45:1039–1041
Cornely OA, Bassetti M, Calandra T, Garbino J, Kullberg BJ, Lortholary O, Meersseman W, Akova M, Arendrup MC, Arikan-Akdagli S, Bille J, Castagnola E, Cuenca-Estrella M, Donnelly JP, Groll AH, Herbrecht R, Hope WW, Jensen HE, Lass-Florl C, Petrikkos G, Richardson MD, Roilides E, Verweij PE, Viscoli C, Ullmann AJ (2012) ESCMID* guideline for the diagnosis and management of Candida diseases 2012: non-neutropenic adult patients. Clin Microbiol Infect 18(Suppl 7):19–37
Craigen MA, Watters J, Hackett JS (1992) The changing epidemiology of osteomyelitis in children. J Bone Joint Surg Br 74:541–545
Crum NF (2004) Bacterial pyomyositis in the United States. Am J Med 117:420–428
Czekaj J, Dinh A, Moldovan A, Vaudaux P, Gras G, Hoffmeyer P, Lew D, Bernard L, Uckay I (2011) Efficacy of a combined oral clindamycin-rifampicin regimen for therapy of staphylococcal osteoarticular infections. Scand J Infect Dis 43:962–967
Dartnell J, Ramachandran M, Katchburian M (2012) Haematogenous acute and subacute paediatric osteomyelitis: a systematic review of the literature. J Bone Joint Surg Br 94:584–595
Davis JS (2005) Management of bone and joint infections due to Staphylococcus aureus. Intern Med J 35(Suppl 2):S79–S96
Desandre AR, Cottone FJ, Evers ML (1995) Iliopsoas abscess: etiology, diagnosis, and treatment. Am Surg 61:1087–1091
Doss M, Martens S, Wood JP, Wolff JD, Baier C, Moritz A (2002) Vacuum-assisted suction drainage versus conventional treatment in the management of poststernotomy osteomyelitis. Eur J Cardiothorac Surg 22:934–938
Dubost JJ, Fis I, Denis P, Lopitaux R, Soubrier M, Ristori JM, Bussiere JL, Sirot J, Sauvezie B (1993) Polyarticular septic arthritis. Medicine (Baltimore) 72:296–310
Dubost JJ, Soubrier M, De Champs C, Ristori JM, Bussiere JL, Sauvezie B (2002) No changes in the distribution of organisms responsible for septic arthritis over a 20 year period. Ann Rheum Dis 61:267–269
El Oakley RM, Wright JE (1996) Postoperative mediastinitis: classification and management. Ann Thorac Surg 61:1030–1036
Elasri MO, Thomas JR, Skinner RA, Blevins JS, Beenken KE, Nelson CL, Smeltzer MS (2002) Staphylococcus aureus collagen adhesin contributes to the pathogenesis of osteomyelitis. Bone 30:275–280
Ellington JK, Reilly SS, Ramp WK, Smeltzer MS, Kellam JF, Hudson MC (1999) Mechanisms of Staphylococcus aureus invasion of cultured osteoblasts. Microb Pathog 26:317–323
Falagas ME, Rosmarakis ES (2006) Recurrent post-sternotomy mediastinitis. J Infect 52:e151–e154
Fuchs T, Schmidmaier G, Raschke MJ, Stange R (2008) Bioactive-coated implants in trauma surgery. Eur J Trauma Emerg Surg 34:60–68
Fuursted K, Arpi M, Lindblad BE, Pedersen LN (2008) Broad-range PCR as a supplement to culture for detection of bacterial pathogens in patients with a clinically diagnosed spinal infection. Scand J Infect Dis 40:772–777
Garzoni C, Kelley WL (2009) Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol 17:59–65
Gasbarrini AL, Bertoldi E, Mazzetti M, Fini L, Terzi S, Gonella F, Mirabile L, Barbanti BG, Furno A, Gasbarrini A, Boriani S (2005) Clinical features, diagnostic and therapeutic approaches to haematogenous vertebral osteomyelitis. Eur Rev Med Pharmacol Sci 9:53–66
Gold RH, Hawkins RA, Katz RD (1991) Bacterial osteomyelitis: findings on plain radiography, CT, MR, and scintigraphy. AJR Am J Roentgenol 157:365–370
Goldenberg DL (1998) Septic arthritis. Lancet 351:197–202
Goldenberg DL, Reed JI (1985) Bacterial arthritis. N Engl J Med 312:764–771
Gordon BA, Martinez S, Collins AJ (1995) Pyomyositis: characteristics at CT and MR imaging. Radiology 197:279–286
Grammatico L, Baron S, Rusch E, Lepage B, Surer N, Desenclos JC, Besnier JM (2008) Epidemiology of vertebral osteomyelitis (VO) in France: analysis of hospital-discharge data 2002–2003. Epidemiol Infect 136:653–660
Gross T, Kaim AH, Regazzoni P, Widmer AF (2002) Current concepts in posttraumatic osteomyelitis: a diagnostic challenge with new imaging options. J Trauma 52:1210–1219
Grossi EA, Culliford AT, Krieger KH, Kloth D, Press R, Baumann FG, Spencer FC (1985) A survey of 77 major infectious complications of median sternotomy: a review of 7,949 consecutive operative procedures. Ann Thorac Surg 40:214–223
Gummert JF, Barten MJ, Hans C, Kluge M, Doll N, Walther T, Hentschel B, Schmitt DV, Mohr FW, Diegeler A (2002) Mediastinitis and cardiac surgery—an updated risk factor analysis in 10,373 consecutive adult patients. Thorac Cardiovasc Surg 50:87–91
Gupta MN, Sturrock RD, Field M (2001) A prospective 2-year study of 75 patients with adult-onset septic arthritis. Rheumatology (Oxford) 40:24–30
Gupta A, Kowalski TJ, Osmon DR, Enzler M, Steckelberg JM, Huddleston PM, Nassr A, Mandrekar JM, Berbari EF (2014) Long-term outcome of pyogenic vertebral osteomyelitis: a cohort study of 260 patients. Open Forum Infect Dis 1:ofu107
Habib G, Lancellotti P, Antunes MJ, Bongiorni MG, Casalta JP, Del Zotti F., Dulgheru R, El KG, Erba PA, Iung B, Miro JM, Mulder BJ, Plonska-Gosciniak E, Price S, Roos-Hesselink J, Snygg-Martin U, Thuny F, Tornos MP, Vilacosta I, Zamorano JL (2015) 2015 ESC guidelines for the management of infective endocarditis: the task force for the management of infective endocarditis of the European Society of Cardiology (ESC) endorsed by: European Association for Cardio-Thoracic Surgery (EACTS), the European Association of Nuclear Medicine (EANM). Eur Heart J 36:3075–3128
Hariharan P, Kabrhel C (2011) Sensitivity of erythrocyte sedimentation rate and C-reactive protein for the exclusion of septic arthritis in emergency department patients. J Emerg Med 40:428–431
Haslinger-Löffler B, Kahl BC, Grundmeier M, Strangfeld K, Wagner B, Fischer U, Cheung AL, Peters G, Schulze-Osthoff K, Sinha B (2005) Multiple virulence factors are required for Staphylococcus aureus-induced apoptosis in endothelial cells. Cell Microbiol 7:1087–1097
Henke PK, Blackburn SA, Wainess RW, Cowan J, Terando A, Proctor M, Wakefield TW, Upchurch GR Jr, Stanley JC, Greenfield LJ (2005) Osteomyelitis of the foot and toe in adults is a surgical disease: conservative management worsens lower extremity salvage. Ann Surg 241:885–892
Hersh RE, Jack JM, Dahman MI, Morgan RF, Drake DB (2001) The vacuum-assisted closure device as a bridge to sternal wound closure. Ann Plast Surg 46:250–254
Horst SA, Hoerr V, Beineke A, Kreis C, Tuchscherr L, Kalinka J, Lehne S, Schleicher I, Köhler G, Fuchs T, Raschke MJ, Rohde M, Peters G, Faber C, Löffler B, Medina E (2012) A novel mouse model of Staphylococcus aureus chronic osteomyelitis that closely mimics the human infection: an integrated view of disease pathogenesis. Am J Pathol 181:1206–1214
Howard AW, Viskontas D, Sabbagh C (1999) Reduction in osteomyelitis and septic arthritis related to Haemophilus influenzae type B vaccination. J Pediatr Orthop 19:705–709
Howard-Jones AR, Isaacs D (2010) Systematic review of systemic antibiotic treatment for children with chronic and sub-acute pyogenic osteomyelitis. J Paediatr Child Health 46:736–741
Hsueh PR, Hsiue TR, Hsieh WC (1996) Pyomyositis in intravenous drug abusers: report of a unique case and review of the literature. Clin Infect Dis 22:858–860
Hughes JG, Vetter EA, Patel R, Schleck CD, Harmsen S, Turgeant LT, Cockerill FR III (2001) Culture with BACTEC Peds Plus/F bottle compared with conventional methods for detection of bacteria in synovial fluid. J Clin Microbiol 39:4468–4471
Idusuyi OB (2015) Surgical management of Charcot neuroarthropathy. Prosthet Orthot Int 39:61–72
Jagodzinski NA, Kanwar R, Graham K, Bache CE (2009) Prospective evaluation of a shortened regimen of treatment for acute osteomyelitis and septic arthritis in children. J Pediatr Orthop 29:518–525
Jaramillo D (2011) Infection: musculoskeletal. Pediatr Radiol 41(Suppl 1):S127–S134
Join-Lambert O, Ribadeau-Dumas F, Jullien V, Kitzis MD, Jais JP, Coignard-Biehler H, Guet-Revillet H, Consigny PH, Delage M, Nassif X, Lortholary O, Nassif A (2014) Dramatic reduction of clindamycin plasma concentration in hidradenitis suppurativa patients treated with the rifampin-clindamycin combination. Eur J Dermatol 24:94–95
Julian OC, Lopez-Belio M, Dye WS, Javid H, Grove WJ (1957) The median sternal incision in intracardiac surgery with extracorporeal circulation; a general evaluation of its use in heart surgery. Surgery 42:753–761
Jurkiewicz MJ, Bostwick J III, Hester TR, Bishop JB, Craver J (1980) Infected median sternotomy wound. Successful treatment by muscle flaps. Ann Surg 191:738–744
Kaandorp CJ, van Schaardenburg D, Krijnen P, Habbema JD, van de Laar MA (1995) Risk factors for septic arthritis in patients with joint disease. A prospective study. Arthritis Rheum 38:1819–1825
Kaandorp CJ, Dinant HJ, van de Laar MA, Moens HJ, Prins AP, Dijkmans BA (1997a) Incidence and sources of native and prosthetic joint infection: a community based prospective survey. Ann Rheum Dis 56:470–475
Kaandorp CJ, Krijnen P, Moens HJ, Habbema JD, van SD (1997b) The outcome of bacterial arthritis: a prospective community-based study. Arthritis Rheum 40:884–892
Kalinka J, Hachmeister M, Geraci J, Sordelli D, Hansen U, Niemann S, Oetermann S, Peters G, Löffler B, Tuchscherr L (2014) Staphylococcus aureus isolates from chronic osteomyelitis are characterized by high host cell invasion and intracellular adaptation, but still induce inflammation. Int J Med Microbiol 304:1038–1049
Kim H, Kim J, Ihm C (2010) The usefulness of multiplex PCR for the identification of bacteria in joint infection. J Clin Lab Anal 24:175–181
Kim CJ, Song KH, Park WB, Kim ES, Park SW, Kim HB, Oh MD, Kim NJ (2012) Microbiologically and clinically diagnosed vertebral osteomyelitis: impact of prior antibiotic exposure. Antimicrob Agents Chemother 56:2122–2124
Klesius AA, Dzemali O, Simon A, Kleine P, Abdel-Rahman U, Herzog C, Wimmer-Greinecker G, Moritz A (2004) Successful treatment of deep sternal infections following open heart surgery by bilateral pectoralis major flaps. Eur J Cardiothorac Surg 25:218–223
Kortekangas P, Aro HT, Lehtonen OP (1995) Synovial fluid culture and blood culture in acute arthritis. A multi-case report of 90 patients. Scand J Rheumatol 24:44–47
Kowalski TJ, Berbari EF, Huddleston PM, Steckelberg JM, Osmon DR (2006) Do follow-up imaging examinations provide useful prognostic information in patients with spine infection? Clin Infect Dis 43:172–179
Kriegeskorte A, König S, Sander G, Pirkl A, Mahabir E, Proctor RA, von Eiff C, Peters G, Becker K (2011) Small colony variants of Staphylococcus aureus reveal distinct protein profiles. Proteomics 11:2476–2490
Levin MJ, Gardner P, Waldvogel FA (1971) Tropical pyomyositis—an unusual infection due to staphylococcus aureus. N Engl J Med 284:196–198
Lew DP, Waldvogel FA (2004) Osteomyelitis. Lancet 364:369–379
Loop FD, Lytle BW, Cosgrove DM, Mahfood S, McHenry MC, Goormastic M, Stewart RW, Golding LA, Taylor PC (1990) Sternal wound complications after isolated coronary artery bypass grafting: early and late mortality, morbidity, and cost of care. Ann Thorac Surg 49:179–186
Losanoff JE, Richman BW, Jones JW (2002) Disruption and infection of median sternotomy: a comprehensive review. Eur J Cardiothorac Surg 21:831–839
Love C, Palestro CJ (2016) Nuclear medicine imaging of bone infections. Clin Radiol
Mader JT, Shirtliff M, Calhoun JH (1997) Staging and staging application in osteomyelitis. Clin Infect Dis 25:1303–1309
Malcius D, Trumpulyte G, Barauskas V, Kilda A (2005) Two decades of acute hematogenous osteomyelitis in children: are there any changes? Pediatr Surg Int 21:356–359
Malizos K, Sarma J, Seaton RA, Militz M, Menichetti F, Riccio G, Gaudias J, Trostmann U, Pathan R, Hamed K (2016) Daptomycin for the treatment of osteomyelitis and orthopaedic device infections: real-world clinical experience from a European registry. Eur J Clin Microbiol Infect Dis 35:111–118
Margaretten ME, Kohlwes J, Moore D, Bent S (2007) Does this adult patient have septic arthritis? JAMA 297:1478–1488
Marschall J, Bhavan KP, Olsen MA, Fraser VJ, Wright NM, Warren DK (2011) The impact of prebiopsy antibiotics on pathogen recovery in hematogenous vertebral osteomyelitis. Clin Infect Dis 52:867–872
Masquelet AC, Begue T (2010) The concept of induced membrane for reconstruction of long bone defects. Orthop Clin North Am 41:27–37
Mathews CJ, Weston VC, Jones A, Field M, Coakley G (2010) Bacterial septic arthritis in adults. Lancet 375:846–855
McHenry MC, Easley KA, Locker GA (2002) Vertebral osteomyelitis: long-term outcome for 253 patients from 7 Cleveland-area hospitals. Clin Infect Dis 34:1342–1350
McKee MD, Wild LM, Schemitsch EH, Waddell JP (2002) The use of an antibiotic-impregnated, osteoconductive, bioabsorbable bone substitute in the treatment of infected long bone defects: early results of a prospective trial. J Orthop Trauma 16:622–627
McKee MD, Li-Bland EA, Wild LM, Schemitsch EH (2010) A prospective, randomized clinical trial comparing an antibiotic-impregnated bioabsorbable bone substitute with standard antibiotic-impregnated cement beads in the treatment of chronic osteomyelitis and infected nonunion. J Orthop Trauma 24:483–490
Merritt K (1988) Factors increasing the risk of infection in patients with open fractures. J Trauma 28:823–827
Milano CA, Georgiade G, Muhlbaier LH, Smith PK, Wolfe WG (1999) Comparison of omental and pectoralis flaps for poststernotomy mediastinitis. Ann Thorac Surg 67:377–380
Mitchell G, Fugere A, Pepin Gaudreau K, Brouillette E, Frost EH, Cantin AM, Malouin F (2013) SigB is a dominant regulator of virulence in Staphylococcus aureus small-colony variants. PLoS ONE 8:e65018
Miyake H (1904) Beitrag zur Kenntniss des sogenannten Myositis infectiosa. Mitt Grenzgeb Med Chir 13:145–198
Mylona E, Samarkos M, Kakalou E, Fanourgiakis P, Skoutelis A (2009) Pyogenic vertebral osteomyelitis: a systematic review of clinical characteristics. Semin Arthritis Rheum 39:10–17
Nahai F, Rand RP, Hester TR, Bostwick J III, Jurkiewicz MJ (1989) Primary treatment of the infected sternotomy wound with muscle flaps: a review of 211 consecutive cases. Plast Reconstr Surg 84:434–441
Neut D, Kluin OS, Crielaard BJ, van der Mei HC, Busscher HJ, Grijpma DW (2009) A biodegradable antibiotic delivery system based on poly-(trimethylene carbonate) for the treatment of osteomyelitis. Acta Orthop 80:514–519
Novick R (2000) Pathogenicity factors and their regulation. In: Fischetti VA (ed) Gram-positive pathogens. American Society of Microbiology, Washington, D.C., pp 392–407
Novick RP (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48:1429–1449
Osmon DR, Berbari EF, Berendt AR, Lew D, Zimmerli W, Steckelberg JM, Rao N, Hanssen A, Wilson WR (2013) Diagnosis and management of prosthetic joint infection: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis 56:e1–e25
Otto M (2009) Staphylococcus epidermidis—the ‘accidental’ pathogen. Nat Rev Microbiol 7:555–567
Otto MP, Martin E, Badiou C, Lebrun S, Bes M, Vandenesch F, Etienne J, Lina G, Dumitrescu O (2013) Effects of subinhibitory concentrations of antibiotics on virulence factor expression by community-acquired methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 68:1524–1532
Parsons B, Strauss E (2004) Surgical management of chronic osteomyelitis. Am J Surg 188:57–66
Patzakis MJ, Wilkins J (1989) Factors influencing infection rate in open fracture wounds. Clin Orthop Relat Res 36–40
Peltola H, Pääkkönen M (2014) Acute osteomyelitis in children. N Engl J Med 370:352–360
Peltola H, Pääkkönen M, Kallio P, Kallio MJ (2010) Short- versus long-term antimicrobial treatment for acute hematogenous osteomyelitis of childhood: prospective, randomized trial on 131 culture-positive cases. Pediatr Infect Dis J 29:1123–1128
Peterson TC, Pearson C, Zekaj M, Hudson I, Fakhouri G, Vaidya R (2014) Septic arthritis in intravenous drug abusers: a historical comparison of habits and pathogens. J Emerg Med 47:723–728
Pfeifer R, Kobbe P, Knobe M, Pape HC (2011) The reamer-irrigator-aspirator (RIA) system. Oper Orthop Traumatol 23:446–452
Pigrau C, Almirante B, Flores X, Falco V, Rodriguez D, Gasser I, Villanueva C, Pahissa A (2005) Spontaneous pyogenic vertebral osteomyelitis and endocarditis: incidence, risk factors, and outcome. Am J Med 118:1287
Proctor RA, van Langevelde P, Kristjansson M, Maslow JN, Arbeit RD (1995) Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin Infect Dis 20:95–102
Proctor RA, von Eiff C, Kahl BC, Becker K, McNamara P, Herrmann M, Peters G (2006) Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4:295–305
Raschke MJ, Schmidmaier G (2004) Biological coating of implants in trauma and orthopedic surgery. Unfallchirurg 107:653–663
Rasigade JP, Trouillet-Assant S, Ferry T, Diep BA, Sapin A, Lhoste Y, Ranfaing J, Badiou C, Benito Y, Bes M, Couzon F, Tigaud S, Lina G, Etienne J, Vandenesch F, Laurent F (2013) PSMs of hypervirulent Staphylococcus aureus act as intracellular toxins that kill infected osteoblasts. PLoS ONE 8:e63176
Reichert P, Rutowski R, Zimmer K, Gosk J (2007) Application of gentamycini impregnated polymethylmethacrylate (PMMA) (Septopal) in treatment of infected nonunion. Own experiments. Polim Med 37:65–72
Ricci MA, Rose FB, Meyer KK (1986) Pyogenic psoas abscess: worldwide variations in etiology. World J Surg 10:834–843
Riise OR, Kirkhus E, Handeland KS, Flato B, Reiseter T, Cvancarova M, Nakstad B, Wathne KO (2008) Childhood osteomyelitis-incidence and differentiation from other acute onset musculoskeletal features in a population-based study. BMC Pediatr 8:45
Ringelman PR, Vander Kolk CA, Cameron D, Baumgartner WA, Manson PN (1994) Long-term results of flap reconstruction in median sternotomy wound infections. Plast Reconstr Surg 93:1208–1214
Robicsek F, Daugherty HK, Cook JW (1977) The prevention and treatment of sternum separation following open-heart surgery. J Thorac Cardiovasc Surg 73:267–268
Roblot F, Besnier JM, Juhel L, Vidal C, Ragot S, Bastides F, Le MG, Godet C, Mulleman D, Azais I, Becq-Giraudon B, Choutet P (2007) Optimal duration of antibiotic therapy in vertebral osteomyelitis. Semin Arthritis Rheum 36:269–277
Rodgers WB, Yodlowski ML, Mintzer CM (1993) Pyomyositis in patients who have the human immunodeficiency virus. Case report and review of the literature. J Bone Joint Surg Am 75:588–592
Roux S, Valour F, Karsenty J, Gagnieu MC, Perpoint T, Lustig S, Ader F, Martha B, Laurent F, Chidiac C, Ferry T (2016) Daptomycin >6 mg/kg/day as salvage therapy in patients with complex bone and joint infection: cohort study in a regional reference center. BMC Infect Dis 16:83
Rybak MJ, Lomaestro BM, Rotschafer JC, Moellering RC, Craig WA, Billeter M, Dalovisio JR, Levine DP (2009) Vancomycin therapeutic guidelines: a summary of consensus recommendations from the Infectious Diseases Society of America, the American Society of Health-System Pharmacists, and the Society of Infectious Diseases Pharmacists. Clin Infect Dis 49:325–327
Salar O, Baker B, Kurien T, Taylor A, Moran C (2014) Septic arthritis in the era of immunosuppressive treatments. Ann R Coll Surg Engl 96:e11–e12
Schaumburg F, Peters G, Alabi A, Becker K, Idelevich EA (2016) Missense mutations of PBP2a are associated with reduced susceptibility to ceftaroline and ceftobiprole in African MRSA. J Antimicrob Chemother 71:41–44
Schmidmaier G, Lucke M, Wildemann B, Haas NP, Raschke M (2006) Prophylaxis and treatment of implant-related infections by antibiotic-coated implants: a review. Injury 37(Suppl 2):S105–S112
Schrenzel J, Harbarth S, Schockmel G, Genne D, Bregenzer T, Flueckiger U, Petignat C, Jacobs F, Francioli P, Zimmerli W, Lew DP (2004) A randomized clinical trial to compare fleroxacin-rifampicin with flucloxacillin or vancomycin for the treatment of staphylococcal infection. Clin Infect Dis 39:1285–1292
Seaton RA, Menichetti F, Dalekos G, Beiras-Fernandez A, Nacinovich F, Pathan R, Hamed K (2015) Evaluation of effectiveness and safety of high-dose daptomycin: results from patients included in the European Cubicin® outcomes registry and experience. Adv Ther 32:1192–1205
Sehn JK, Gilula LA (2012) Percutaneous needle biopsy in diagnosis and identification of causative organisms in cases of suspected vertebral osteomyelitis. Eur J Radiol 81:940–946
Sendi P, Zimmerli W (2012) Antimicrobial treatment concepts for orthopaedic device-related infection. Clin Microbiol Infect 18:1176–1184
Shields D, Robinson P, Crowley TP (2012) Iliopsoas abscess—a review and update on the literature. Int J Surg 10:466–469
Shirtliff ME, Mader JT (2002) Acute septic arthritis. Clin Microbiol Rev 15:527–544
Shmerling RH, Delbanco TL, Tosteson AN, Trentham DE (1990) Synovial fluid tests. What should be ordered? JAMA 264:1009–1014
Sinha B, Francois PP, Nusse O, Foti M, Hartford OM, Vaudaux P, Foster TJ, Lew DP, Herrmann M, Krause KH (1999) Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell Microbiol 1:101–117
Stengel D, Bauwens K, Sehouli J, Ekkernkamp A, Porzsolt F (2001) Systematic review and meta-analysis of antibiotic therapy for bone and joint infections. Lancet Infect Dis 1:175–188
Strommenger B, Layer F, Klare I, Werner G (2015) Pre-use susceptibility to ceftaroline in clinical Staphylococcus aureus isolates from Germany: is there a non-susceptible pool to be selected? PLoS ONE 10:e0125864
Tande AJ, Patel R (2014) Prosthetic joint infection. Clin Microbiol Rev 27:302–345
Tebartz C, Horst SA, Sparwasser T, Huehn J, Beineke A, Peters G, Medina E (2015) A major role for myeloid-derived suppressor cells and a minor role for regulatory T cells in immunosuppression during Staphylococcus aureus infection. J Immunol 194:1100–1111
Tegnell A, Arén C, Öhman L (2000) Coagulase-negative staphylococci and sternal infections after cardiac operation. Ann Thorac Surg 69:1104–1109
Tice AD, Hoaglund PA, Shoultz DA (2003) Outcomes of osteomyelitis among patients treated with outpatient parenteral antimicrobial therapy. Am J Med 114:723–728
Torda AJ, Gottlieb T, Bradbury R (1995) Pyogenic vertebral osteomyelitis: analysis of 20 cases and review. Clin Infect Dis 20:320–328
Trampuz A, Zimmerli W (2006a) Antimicrobial agents in orthopaedic surgery: prophylaxis and treatment. Drugs 66:1089–1105
Trampuz A, Zimmerli W (2006b) Diagnosis and treatment of infections associated with fracture-fixation devices. Injury 37(Suppl 2):S59–S66
Tuchscherr L, Löffler B (2016) Staphylococcus aureus dynamically adapts global regulators and virulence factor expression in the course from acute to chronic infection. Curr Genet 62:15–17
Tuchscherr L, Heitmann V, Hussain M, Viemann D, Roth J, von Eiff C, Peters G, Becker K, Löffler B (2010) Staphylococcus aureus small-colony variants are adapted phenotypes for intracellular persistence. J Infect Dis 202:1031–1040
Tuchscherr L, Medina E, Hussain M, Volker W, Heitmann V, Niemann S, Holzinger D, Roth J, Proctor RA, Becker K, Peters G, Löffler B (2011) Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol Med 3:129–141
Tuchscherr L, Bischoff M, Lattar SM, Noto Llana M, Pförtner H, Niemann S, Geraci J, Van de Vyver H, Fraunholz MJ, Cheung AL, Herrmann M, Völker U, Sordelli DO, Peters G, Löffler B (2015) Sigma factor SigB is crucial to mediate Staphylococcus aureus adaptation during chronic infections. PLoS Pathog 11:e1004870
Tuchscherr L, Kreis CA, Hoerr V, Flint L, Hachmeister M, Geraci J, Bremer-Streck S, Kiehntopf M, Medina E, Kribus M, Raschke M, Pletz M, Peters G, Loffler B (2016) Staphylococcus aureus develops increased resistance to antibiotics by forming dynamic small colony variants during chronic osteomyelitis. J Antimicrob Chemother 71:438–448
Tung H, Guss B, Hellman U, Persson L, Rubin K, Ryden C (2000) A bone sialoprotein-binding protein from Staphylococcus aureus: a member of the staphylococcal Sdr family. Biochem J 345(Pt 3):611–619
Uckay I, Gariani K, Pataky Z, Lipsky BA (2014) Diabetic foot infections: state-of-the-art. Diabetes Obes Metab 16:305–316
Uckay I, Aragon-Sanchez J, Lew D, Lipsky BA (2015) Diabetic foot infections: what have we learned in the last 30 years? Int J Infect Dis 40:81–91
Valour F, Rasigade JP, Trouillet-Assant S, Gagnaire J, Bouaziz A, Karsenty J, Lacour C, Bes M, Lustig S, Benet T, Chidiac C, Etienne J, Vandenesch F, Ferry T, Laurent F (2015) Delta-toxin production deficiency in Staphylococcus aureus: a diagnostic marker of bone and joint infection chronicity linked with osteoblast invasion and biofilm formation. Clin Microbiol Infect 21:568
Van Bambeke F, Barcia-Macay M, Lemaire S, Tulkens PM (2006) Cellular pharmacodynamics and pharmacokinetics of antibiotics: current views and perspectives. Curr Opin Drug Discov Devel 9:218–230
Venkatesan K (1992) Pharmacokinetic drug interactions with rifampicin. Clin Pharmacokinet 22:47–65
Viale P, Furlanut M, Scudeller L, Pavan F, Negri C, Crapis M, Zamparini E, Zuiani C, Cristini F, Pea F (2009) Treatment of pyogenic (non-tuberculous) spondylodiscitis with tailored high-dose levofloxacin plus rifampicin. Int J Antimicrob Agents 33:379–382
von Eiff C, Bettin D, Proctor RA, Rolauffs B, Lindner N, Winkelmann W, Peters G (1997a) Recovery of small colony variants of Staphylococcus aureus following gentamicin bead placement for osteomyelitis. Clin Infect Dis 25:1250–1251
von Eiff C, Heilmann C, Proctor RA, Woltz C, Peters G, Götz F (1997b) A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J Bacteriol 179:4706–4712
von Eiff C, Becker K, Machka K, Stammer H, Peters G (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. N Engl J Med 344:11–16
Wagner FW Jr (1981) The dysvascular foot: a system for diagnosis and treatment. Foot Ankle 2:64–122
Waldvogel FA, Medoff G, Swartz MN (1970a) Osteomyelitis: a review of clinical features, therapeutic considerations and unusual aspects. N Engl J Med 282:198–206
Waldvogel FA, Medoff G, Swartz MN (1970b) Osteomyelitis: a review of clinical features, therapeutic considerations and unusual aspects. 3. Osteomyelitis associated with vascular insufficiency. N Engl J Med 282:316–322
Weston VC, Jones AC, Bradbury N, Fawthrop F, Doherty M (1999) Clinical features and outcome of septic arthritis in a single UK Health District 1982–1991. Ann Rheum Dis 58:214–219
Wright JA, Nair SP (2010) Interaction of staphylococci with bone. Int J Med Microbiol 300:193–204
Zieger MM, Dorr U, Schulz RD (1987) Ultrasonography of hip joint effusions. Skeletal Radiol 16:607–611
Ziegler C, Goldmann O, Hobeika E, Geffers R, Peters G, Medina E (2011) The dynamics of T cells during persistent Staphylococcus aureus infection: from antigen-reactivity to in vivo anergy. EMBO Mol Med 3:652–666
Zimmerli W (2010) Vertebral osteomyelitis. N Engl J Med 362:1022–1029
Zimmerli W, Widmer AF, Blatter M, Frei R, Ochsner PE (1998) Role of rifampin for treatment of orthopedic implant-related staphylococcal infections: a randomized controlled trial. Foreign-Body Infection (FBI) study group. JAMA 279:1537–1541
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Idelevich, E.A., Kreis, C., Löffler, B., Peters, G. (2016). Staphylococcus aureus-Associated Musculoskeletal Infections. In: Bagnoli, F., Rappuoli, R., Grandi, G. (eds) Staphylococcus aureus. Current Topics in Microbiology and Immunology, vol 409. Springer, Cham. https://doi.org/10.1007/82_2016_19
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