Bacterial osteomyelitis in adults: Evolving considerations in diagnosis and treatment

American Journal of Medicine

Volumn 101, Issue 5, 1996, Pages 550-561

  Haas, David W ^a   McAndrew, Mark P ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT;

ADULT; BACTERIAL INFECTION; DIFFERENTIAL DIAGNOSIS; HUMAN; HYPERBARIC OXYGEN; MICROBIOLOGY; MIDDLE AGED; OSTEOMYELITIS; RADIOGRAPHY; REVIEW; TREATMENT OUTCOME;

ADULT; ANTI-BACTERIAL AGENTS; BACTERIAL INFECTIONS; DIAGNOSIS, DIFFERENTIAL; HUMANS; HYPERBARIC OXYGENATION; MIDDLE AGED; OSTEOMYELITIS; TREATMENT OUTCOME;

EID: 0030279922     PISSN: 00029343     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9343(96)00260-4     Document Type: Review

References (117)

1. Waldvogel FA, Medoff G, Swartz MN. Osteomyelitis: a review of clinical features, therapeutic considerations and unusual aspects. NEJM. 1970;282:198-206;260-266;316-322.
2. Waldvogel FA, Vasey H. Osteomyelitis: the past decade. NEJM. 1980;303: 360-370.
3. Kahn DS, Pritzker KPH. The pathophysiology of bone infection. Clin Orth Rel Res. 1973;96:12-19.
4. Trueta J. The three types of acute hematogenous osteomyelitis: a clinical and vascular study. J Bone Joint Surg. 1959;41:671-680.
5. Ukwu HN, Graham BS, Latham RH. Acute pubic osteomyelitis in athletes. Clin Infect Dis. 1992;15:636-638.
6. Norden CW, Kennedy E. Experimental osteomyelitis. I. A description of the model. J Infect Dis. 1970;122:410-418.
7. Gristina AG. Biomaterial-centered infection: microbial adhesion versus tissue integration. Science. 1987;237:1588-1595.
8. Mader JT, Brown GL, Guckian JC, et al. A mechanism for the amelioration by hyperbaric oxygen of experimental staphylococcal osteomyelitis in rabbits. J Infect Dis. 1980;142:915-922.
9. Hill C, Mazas F, Flamant R, Evrard J. Prophylactic cefazolin versus placebo in total hip replacement. Lancet. 1981;i:795-797.
10. Doyon F, Evrard J, Mazas F, Hill C. Long-term results of prophylactic cefazolin versus placebo in total hip replacement. Lancet. 1987;i:860.
11. Naylor PT, Myrvik QN, Gristina A. Antibiotic resistance of biomaterial-adherent coagulase-negative and coagulase-positive staphylococci. Clin Orth Rel Res. 1990;261:126-133.
12. Ryden C, Maxe I, Franzen A, et al. Selective binding of bone matrix sialo-protein to Staphylococcus aureus in osteomyelitis. Lancet. 1987;ii:515.
13. Signas C, Raucci G, Jonsson K, et al. Nucleotide sequence of the gene for a fibrinogen-binding protein from Staphylococcus aureus: use of this peptide sequence in the synthesis of biologically active peptides. Proc Natl Acad Sci USA. 1989;86:699-703.
14. Hawiger JS, Hammond DK, Timmons S, Budzynski AZ. Interaction of human fibrinogen with staphylococci: presence of a binding region on normal and abnormal fibrinogen variants and fibrinogen derivatives. Blood. 1978;51:799-812.
15. Foster TJ, McDevitt D. Surface-associated proteins of Staphylococcus aureus: their possible roles in virulence. FEMS Microbiol Letters. 1994;118:199-205.
16. Patti JM, Jonsson J, Guss B, et al. Molecular characterization and expression of a gene encoding a Staphylococcus aureus collagen adhesion. J Biol Chem. 1992;267:4766-4772.
17. Patti JM, Bremell T, Karjewska-Pietrasik D, et al. The Staphylococcus aureus collagen adhesion is a virulence determinant in experimental septic arthritis. Infect Immun. 1994;62:152-161.
18. Rogolsky M. Nonenteric toxins of Staphylococcus aureus. Microbiol Rev. 1979;43:320.
19. Hung LHY, Norwood LA. Osteomyelitis due to Pseudallescheria boydii. South Med J. 1993;86:231-234.
20. Engh CA, Hughes JL, Abrams RC, Bowerman JW. Osteomyelitis in the patient with sickle-cell disease: diagnosis and management. J Bone Joint Surg. 1971;53:1-15.
21. Meier DE, Tarpley JL, Olaolorun DA, et al. Hematogenous osteomyelitis in the developing world: a practical approach to classification and treatment with limited resources. Contemp Orthoped. 1993;26:495-505.
22. Epps CH, Bryant DD, Coles MJ, Castro O. Osteomyelitis in patients who have sickle-cell disease: diagnosis and treatment. J Bone Joint Surg. 1991;73:1281-1294.
23. Meyers BR, Berson BL, Gilbert M, Hirschman SZ. Clinical patterns of osteomyelitis due to gram-negative bacteria. Arch Intern Med. 1973;131:228-233.
24. DeBoer RG, Dumler M. Pasteurella multocida infections. Am J Clin Pathol. 1963;40:339-344.
25. Ellis ME, Smith CC, Moffatt MAJ. Chronic or fatal Q-fever infection: a review of 16 patients seen in North-East Scotland (1967-1980). Q J Med. 1983;205:54-66.
26. Rubin J, Yu VL. Malignant external otitis: insights into pathogenesis, clinical manifestations, diagnosis, and therapy. Am J Med. 1988;85:391-398.
27. Bamberger DM, Daus GP, Gerding DN. Osteomyelitis in the feet of diabetic patients. Am J Med. 1987;83:653-660.
28. Louie TJ, Bartlett JG, Tally FP, Gorbach SL. Aerobic and anaerobic bacteria in diabetic foot ulcers. Ann Intern Med. 1976;85:461-463.
29. Sapico FL, Canawati HN, Witte JL, et al. Quantitative aerobic and anaerobic bacteriology of infected diabetic feet. J Clin Microbiol. 1980;12:413-420.
30. Sapico FL, Witte JL, Canawati HN, et al. The infected foot of the diabetic patient: quantitative microbiology and analysis of clinical features. Rev Infect Dis. 1984;6:s171-176.
31. Borrero E, Rossini M Jr. Bacteriology of 100 consecutive diabetic foot infections and in vitro susceptibility to ampicillin/sulbactam versus cefoxitin. Angiology. 1992;357-361.
32. Nakata MM, Lewis RP. Anaerobic bacteria in bone and joint infections. Rev Infect Dis. 1984;6:s165-170.
33. Raff MJ, Melo JC. Anaerobic osteomyelitis. Medicine. 1978;57:83-103.
34. Schauwecker DS. The scintigraphic diagnosis of osteomyelitis. AJR. 1992;158:9-18.
35. Howie DW, Savage JP, Wilson TG, Paterson D. The technetium phosphate bone scan in the diagnosis of osteomyelitis in childhood. J Bone Joint Surg. 1983;65A:431-437.
36. Thrall JH, Geslien GE, Corcoron RJ, Johnson MC. Abnormal radionuclide deposition patterns adjacent to focal skeletal lesions. Radiology. 1975;115: 659-663.
37. Alazraki N, Dries D, Datz F, et al. A. Value of a 24-hour image (four-phase bone scan) in assessing osteomyelitis in patients with peripheral vascular disease. J Nucl Med. 1985;26:711-717.
38. Gilday DL, Paul DJ, Paterson J. Diagnosis of osteomyelitis in children by combined blood pool and bone imaging. Radiology. 1975;117:331-335.
39. Majd M, Frankel RS. Radionuclide imaging in skeletal inflammatory and ischemic disease in children. AJR. 1976;126:832-841.
40. Schauwecker DS, Park HM, Mock BH, et al. Evaluation of complicating osteomyelitis with Tc-99m MDP, In-111 granulocytes, and Ga-67 citrate. J Nucl Med. 1984;25:849-853.
41. Ruther W, Hotze A, Moller F, et al. Diagnosis of bone and joint infection by leucocyte scintigraphy: a comparative study with 99mTc-HMPAO-labeled leucocytes, 99mTc-labeled antigranulocyte antibodies and 99mTc-labeled nanocolloid. Arch Orthop Trauma Surg. 1990;110:26-32.
42. 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;266:1246-1251.
43. Seabold JE, Nepola JV, Conrad GR, et al. Detection of osteomyelitis at fracture nonunion sites: comparison of two scintigraphic methods. AJR. 1989;152:1021-1027.
44. Modic MT, Feiglin DH, Piraino DW, et al. Vertebral osteomyelitis: assessment using MRI. Radiology. 1985;157:157-166.
45. Otremski I, Newman RJ, Kahn PJ, et al. Leukergy: a new diagnostic test for bone infection. J Bone Joint Surg. 1993;75:734-736.
46. Sanzen L. The erythrocyte sedimentation rate following exchange of infected total hips. Acta Orthop Scand. 1988;59:148-150.
47. Carlsson AS. Erythrocyte sedimentation rate in infected and non-infected total hip arthroplasties. Acta Orthop Scand. 1978;49:287-290.
48. Sanzen L, Carlsson AS. The diagnostic value of C-reactive protein in infected total hip arthroplasties. J Bone Joint Surg. 1989;71B:638-641.
49. Smith CW, Marlin SD, Rothlein R, et al. Cooperative interactions of LFA-1 and Mac-1 with intercellular adhesion molecule-1 in facilitating adherence and transendothelial migration of human neutrophils in vitro. J Clin Invest. 1989;83:2008-2017.
50. Williams RC Jr, Dossett JH, Quie PG. Comparative studies of immunoglobulin opsonins in osteomyelitis and other established infections, Immunology. 1969;17:249-265.
51. Wergeland HI, Haaheim LR, Natas OB, et al. Antibodies to staphylococcal peptidoglycan and its peptide epitopes, teichoic acid, and lipoteichoic acid in sera from blood donors and patients with staphylococcal infections. J Clin Microbiol. 1989;27:1286-1291.
52. Lambert PA, Krikler SJ, Patel R, Parvathan S. Enzyme-linked immunosorbent assay for the detection of antibodies to exocellular proteins of Staphylococcus aureus in bone infection. FEMS Microbiol Letters. 1992;100:67-70.
53. Mackowiak PA, Jones SR, Smith JW. Diagnostic value of sinus-tract cultures in chronic osteomyelitis. JAMA. 1978;239:2772-2775.
54. Wheat J. Diagnostic strategies in osteomyelitis. Am J Med. 1985;78(suppl 6B):218-224.
55. 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. 1991;73-A:745-749.
56. Hofer M, Hirschel B, Kirschner P, et al. Disseminated osteomyelitis from Mycobacterium ulcerans after a snakebite. NEJM. 1993;328:1007-1009.
57. Weinstein MP, Stratton CW, Hawley HB, et al. Multicenter collaborative evaluation of a standardized serum bactericidal test as a predictor of therapeutic efficacy in acute and chronic osteomyelitis. Am J Med. 1987;83:218-222.
58. Norden CW, Bryant R, Palmer D, et al. Chronic osteomyelitis caused by Staphylococcus aureus: controlled clinical trial of nafcillin therapy and nafcillin-rifampin therapy. South Med J. 1986;79:947-951.
59. Sheftel TG, Mader JT. Randomized evaluation of ceftazidime or ticarcillin and tobramycin for the treatment of osteomyelitis caused by gram-negative bacilli. Antimicrob Agents Chemother. 1986;29:112-115.
60. Mader JT, Cantrell JS, Calhoun J. Oral ciprofloxacin compared with standard parenteral antibiotic therapy for chronic osteomyelitis in adults. J Bone Joint Surg. 1990;72A:104-110.
61. Gentry LO, Rodriguez-Gomez G. Oral ciprofloxacin compared with parenteral antibiotics in the treatment of osteomyelitis. Antimicrob Agents Chemother. 1990;34:40-43.
62. Gentry LO, Rodriguez-Gomez G. Ofloxacin versus parenteral therapy for chronic osteomyelitis. Antimicrob Agents Chemother. 1991;35:538-541.
63. Norden CW. Experimental osteomyelitis. IV. Therapeutic trials with rifampin alone and in combination with gentamicin, sisomicin, and cephalothin. J Infect Dis. 1975;132:493-499.
64. Norden CW. Experimental chronic staphylococcal osteomyelitis in rabbits: treatment with rifampin alone and in combination with other antimicrobial agents. Rev Infect Dis. 1983;5:S491-494.
65. Norden CW, Keleti E. Treatment of experimental staphylococcal osteomyelitis with rifampin and trimethoprim, alone and in combination. Antimicrob Agents Chemother. 1980;17:591-594.
66. Norden CW, Shinners E, Niederriter K. Clindamycin treatment of experimental chronic osteomyelitis due to Staphylococcus aureus. J Infect Dis. 1986;153:956-959.
67. Norden CW, Budinsky A. Treatment of experimental chronic osteomyelitis due to Staphylococcus aureus with ampicillin/sulbactam. J Infect Dis. 1990;161:52-53.
68. Norden CW. Osteomyelitis. In: Mandell GL, Douglas RG, Bennett JE, eds. Principles and Practice of Infectious Diseases. 4th ed. New York: Churchill Livingstone; 1990:922-930.
69. Chow JW, Fine MJ, Shlaes DM, et al. Enterobacter bacteremia: clinical features and emergence of antibiotic resistance during therapy. Ann Intern Med. 1991;115:585-590.
70. Gentry LO. Oral antimicrobial therapy for osteomyelitis. Ann Intern Med. 1991;114:986-987.
71. Blumberg HM. Oral quinolone treatment for osteomyelitis. Ann Intern Med. 1991;115:832.
72. Drancourt M, Stein A, Argenson JN, Zannier A, Curvale G, Raoult D. Oral rifampin plus ofloxacin for treatment of Staphylococcus-infected orthopedic implants. Antimicrob Agents Chemother. 1993;37:1214-1218.
73. Cramer JA, Mattson RH, Prevey ML, et al. How often is medication taken as prescribed? JAMA 1989;261:3273-3277.
74. Cramer JA, Scheyer RD, Mattson RH. Compliance between clinic visits. Arch Intern Med 1990;150:1509-1510.
75. Cierny G III, Mader JT. Approach to adult osteomyelitis. Orthop Rev. 1987;16:259-270.
76. Swiontkowski MF. Criteria for bone debridement in massive lower limb trauma. Clin Orth Rel Res. 1989;243:41-47.
77. Duwelius PJ, Schmidt AH. Assessment of bone viability in patients with osteomyelitis: preliminary clinical experience with laser doppler flowmetry. J Orthop Trauma. 1992;6:327-332.
78. Weiland AJ, Moore JR, Daniel RK. Vascularized bone autografts: experience with 41 cases. Clin Orth Rel Res. 1983;174:87-95.
79. Ilizarov GA. The tension-stress effect on the genesis and growth of tissues: Part I. The influence of stability of fixation and soft-tissue preservation. Clin Orth Rel Res. 1989;238:249-281.
80. Ilizarov GA. The tension-stress effect on the genesis and growth of tissues: Part II. The influence of the rate and frequency of distraction. Clin Orth Rel Res. 1989;239:263-285.
81. Nusbickel FR, Dell PC, McAndrew MP, Moore MM. Vascularized autografts for reconstruction of skeletal defects following lower extremity trauma: a review. Clin Orth Rel Res. 1989;243:65-70.
82. Brumback RJ, McBride MS, Ortolani NC. Functional evaluation of the shoulder after transfer of the vascularized latissimus dorsi muscle. J Bone Joint Surg. 1992;74A:377-382.
83. Gore DR, Gardner GM, Sepic SB, et al. Function following partial fibulectomy. Clin Orth Rel Res. 1987;220:206-210.
84. Youdas JW, Wood MB, Cahalan TD, Chao EY. A quantitative analysis of donor site morbidity after vascularized fibula transfer. J Orthop Res. 1988;6:621-629.
85. Goodacre TE, Walker CJ, Jawad AS, et al. Donor site morbidity following osteocutaneous free fibula transfer. Br J Plastic Surg. 1990;43:410-412.
86. Calhoun JH, Mader JT. Antibiotic beads in the management of surgical infections. Am J Surg. 1989;157:443-449.
87. Tong Y, Wei X, Qiu G, et al. The treatment of chronic hematogenous osteomyelitis. Clin Orthop. 1987;215:72-77.
88. Dahners LE, Funderburk CH. Gentamicin-loaded plaster of Paris as a treatment of experimental osteomyelitis in rabbits. Clin Orthop. 1987;219:278-282.
89. Zilch H, Lambiris E. The sustained release of cefotaxim from a fibrin-cefotaxim compound in treatment of osteitis. Arch Orthop Trauma Surg. 1986;106:36-41.
90. Ascherl R, Stemberger A, Lechner F, et al. Behandlung der chronischen osteomyelitis mit einem kollagen-antibiotika-verbund-vorlaufige mitteilung. Unfallchirurgie. 1986;12:125-127.
91. Korkusuz F, Uchida A, Shinto Y, et al. Experimental implant-related osteomyelitis treated by antibiotic-calcium hydroxyapatite ceramic composites. J Bone Joint Surg 1993;756:111-114.
92. Duncan CP, Masri BA. The role of antibiotic-loaded cement in the treatment of an infection after a hip replacement. J Bone Joint Surg. 1994;76A:1742-1751.
93. Klecamp JW, Haas DW, DeBoer D, et al. Biomechanical effects, elution kinetics and antibacterial activities of vancomycin and tobramycin in polymethylmethacrylate, and effects of vacuum mixing. Presented at the Fourth Annual Meeting of the Musculoskeletal Infection Society, Snowmass, Colorado, 1995.
94. Torholm C, Lindgren L, Lindberg L, Kahlmeter G. Total hip joint arthroplasty with gentamicin-impregnated cement. Clin Orthop Rel Res. 1983;181:99-106.
95. Murray WR. Use of antibiotic-containing bone cement. Clin Orthop. 1984;190:89-95.
96. Lautenschlager EP, Jacobs JJ, Marshall GW, Meyer PR. Mechanical properties of bone cements containing large doses of antibiotic powders. J Biomed Mater Res. 1976;10:929-938.
97. Nelson RC, Hoffman RO, Burton TA. The effect of antibiotic additions on the mechanical properties of acrylic cement. J Biomed Mater Res. 1978; 12:473-490.
98. Davies J, O'Connor DO, Harris WH. Comparison of the mechanical properties of Palacos, Palacos-gentamicin and Simplex P. Orthop Trans. 1984; 8:400-401.
99. Goodell JA, Flick AB, Hebert JC, Howe JG. Preparation and release characteristics of tobramycin-impregnated polymethylmethacrylate beads. Am J Hosp Pharm. 1986;43:1454-1461.
100. Flick AB, Hebert JC, Goodell J, Kristiansen T. Noncommercial fabrication of antibiotic-impregnated polymethylmethacrylate beads: technical notes. Clin Orthop Rel Res. 1987;223:282-286.
101. Kirkpatrick DK, Trachtenbert LS, Mangino PD, et al. In vitro characteristics of tobramycin-PMMA beads; compressive strength and leaching. Orthopaedics. 1985;8:1130-1133.
102. Josefsson G, Lindberg L, Wiklander B. Systemic antibiotics and gentamicin-containing bone cement in the prophylaxis of postoperative infections in total hip arthroplasty. Clin Orthop Rel Res. 1981;159:194-200,
103. Buchholz HW, Elson RA, Engelbrecht E, et al. Management of deep infection of total hip replacement. J Bone Joint Surg 1981;63B:342-353.
104. Lynch M, Esser MP, Shelley P, Wroblewski BM. Deep infection in Charnley low-friction arthroplasty: comparison of plain and gentamicin-loaded cement. J Bone Joint Surg 1987;69B:355-360.
105. Walenkamp GM, Vree TB, Rens TV. Gentamicin-PMMA beads, pharmacokinetic and nephrotoxicologic study. Clin Orthop. 1986;205:171-183.
106. Majid SA, Lindberg LT, Gunterberg B, Siddiki MS. Gentamicin-PMMA beads in the treatment of chronic osteomyelitis. Acta Orthop Scand. 1985;56:265-268.
107. Grieben A. Results of septopal in more than 1500 cases of bone and soft tissue infections: a review of clinical trials. J Bone Joint Surg 1980;62:275-276.
108. Slack WK, Thomas DA, Perrins D. Hyperbaric oxygen in chronic osteomyelitis. Lancet. 1965;i:1093-1094.
109. Hopkinson WI, Towers AG. Effects of hyperbaric oxygen on some common pathogenic bacteria. Lancet. 1963;2:1361-1363.
110. Hill GB, Osterhout S. Experimental effects of hyperbaric oxygen on selected clostridial species. I. In vitro studies. J Infect Dis. 1972;125:17-25.
111. Shaw JL, Bassett CA. The effects of varying oxygen concentrations on osteogenesis and embryonic cartilage in vitro. J Bone Joint Surg. 1967; 49A:73-80.
112. Perrins DJD, Maudsley RH, Colwill RR. OHP in the management of chronic osteomyelitis. In: Brown IW, Cox BG, eds. Proceedings of the Third International Conference on Hyperbaric Medicine. Washington, DC: National Academy of Science, National Research Council, 1966:578-584.
113. Depenbusch FL, Thompson RE, Hart GB. Use of hyperbaric oxygen in the treatment of refractory osteomyelitis: a preliminary report. J Trauma. 1972;12:807-812.
114. Morrey BF, Dunn JM, Heimbach RD, Davis J. Hyperbaric oxygen and chronic osteomyelitis. Clin Orth Rel Res. 1979;144:121-127.
115. Davis JC, Heckman JD, DeLee JC, Buckwold FJ. Chronic non-hematogenous osteomyelitis treated with adjuvant hyperbaric oxygen. J Bone Joint Surg. 1986;68:1210-1217.
116. Esterhai JL Jr, Pisarello J, Brighton CT, et al. Adjunctive hyperbaric oxygen therapy in the treatment of chronic refractory osteomyelitis. J Trauma. 1987;27:763-768.
117. Calhoun JH, Cobos JA, Mader JT. Does hyperbaric oxygen have a place in the treatment of osteomyelitis? Orth Clin North Am. 1991;22:467-471.