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Published in: EJNMMI Research 1/2014

Open Access 01-12-2014 | Original research

68Ga-DOTA-Siglec-9 PET/CT imaging of peri-implant tissue responses and staphylococcal infections

Authors: Helena Ahtinen, Julia Kulkova, Laura Lindholm, Erkki Eerola, Antti J Hakanen, Niko Moritz, Mirva Söderström, Tiina Saanijoki, Sirpa Jalkanen, Anne Roivainen, Hannu T Aro

Published in: EJNMMI Research | Issue 1/2014

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Abstract

Background

Staphylococcus epidermidis (S. epidermidis) has emerged as one of the leading pathogens of biomaterial-related infections. Vascular adhesion protein-1 (VAP-1) is an inflammation-inducible endothelial molecule controlling extravasation of leukocytes. Sialic acid-binding immunoglobulin-like lectin 9 (Siglec-9) is a leukocyte ligand of VAP-1. We hypothesized that 68Ga-labeled 1,4,7,10-tetraazacyclododecane-1,4,7,10-tetraacetic acid-conjugated Siglec-9 motif containing peptide (68Ga-DOTA-Siglec-9) could detect inflammatory response due to S. epidermidis peri-implant infection by positron emission tomography (PET).

Methods

Thirty Sprague-Dawley rats were randomized into three groups. A sterile catheter was implanted into the medullary canal of the left tibia. In groups 1 and 2, the implantation was followed by peri-implant injection of S. epidermidis or Staphylococcus aureus (S. aureus) with adjunct injections of aqueous sodium morrhuate. In group 3, sterile saline was injected instead of bacteria and no aqueous sodium morrhuate was used. At 2 weeks after operation, 68Ga-DOTA-Siglec-9 PET coupled with computed tomography (CT) was performed with the measurement of the standardized uptake value (SUV). The presence of the implant-related infection was verified by microbiological analysis, imaging with fluorescence microscope, and histology. The in vivo PET results were verified by ex vivo measurements by gamma counter.

Results

In group 3, the tibias with implanted sterile catheters showed an increased local uptake of 68Ga-DOTA-Siglec-9 compared with the intact contralateral bones (SUVratio +29.5%). 68Ga-DOTA-Siglec-9 PET detected inflammation induced by S. epidermidis and S. aureus catheter-related bone infections (SUVratio +58.1% and +41.7%, respectively). The tracer uptake was significantly higher in the S. epidermidis group than in group 3 without bacterial inoculation, but the difference between S. epidermidis and S. aureus groups was not statistically significant. The difference between the S. aureus group and group 3 was neither statistically significant.

Conclusion

PET/CT imaging with novel 68Ga-DOTA-Siglec-9 tracer was able to detect inflammatory tissue response induced by catheter implantation and staphylococcal infections.
Appendix
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Literature
1.
go back to reference Zimmerli W, Trampuz A, Ochsner PE: Prosthetic-joint infections. N Engl J Med 2004, 351: 1645–1654. 10.1056/NEJMra040181CrossRefPubMed Zimmerli W, Trampuz A, Ochsner PE: Prosthetic-joint infections. N Engl J Med 2004, 351: 1645–1654. 10.1056/NEJMra040181CrossRefPubMed
2.
go back to reference National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004 Am J Infect Control 2004, 32: 470–485. 10.1016/j.ajic.2004.10.001 National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004 Am J Infect Control 2004, 32: 470–485. 10.1016/j.ajic.2004.10.001
3.
go back to reference Queck SY, Otto M: Staphylococcus epidermidis and other coagulase-negative staphylococci. In Staphycoccus: Molecular Genetics. Edited by: Lindsay JA. Caister Academic Press, Norfolk; 2008:227–254. Queck SY, Otto M: Staphylococcus epidermidis and other coagulase-negative staphylococci. In Staphycoccus: Molecular Genetics. Edited by: Lindsay JA. Caister Academic Press, Norfolk; 2008:227–254.
4.
go back to reference Sadykov MR, Hartmann T, Mattes TA, Hiatt M, Jann NJ, Zhu Y, Ledala N, Landmann R, Herrmann M, Rohde H, Bischoff M, Somerville GA: CcpA coordinates central metabolism and biofilm formation in Staphylococcus epidermidis . Microbiology 2011, 157: 3458–3468. 10.1099/mic.0.051243-0PubMedCentralCrossRefPubMed Sadykov MR, Hartmann T, Mattes TA, Hiatt M, Jann NJ, Zhu Y, Ledala N, Landmann R, Herrmann M, Rohde H, Bischoff M, Somerville GA: CcpA coordinates central metabolism and biofilm formation in Staphylococcus epidermidis . Microbiology 2011, 157: 3458–3468. 10.1099/mic.0.051243-0PubMedCentralCrossRefPubMed
5.
go back to reference von Eiff C, Peters G, Heilmann C: Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2002, 2: 677–685. 10.1016/S1473-3099(02)00438-3CrossRefPubMed von Eiff C, Peters G, Heilmann C: Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2002, 2: 677–685. 10.1016/S1473-3099(02)00438-3CrossRefPubMed
6.
go back to reference Kwakman PH, te Velde AA, Vandenbroucke-Grauls CM, van Deventer SJ, Zaat SA: Treatment and prevention of Staphylococcus epidermidis experimental biomaterial-associated infection by bactericidal peptide 2. Antimicrob Agents Chemother 2006, 50: 3977–3983. 10.1128/AAC.00575-06PubMedCentralCrossRefPubMed Kwakman PH, te Velde AA, Vandenbroucke-Grauls CM, van Deventer SJ, Zaat SA: Treatment and prevention of Staphylococcus epidermidis experimental biomaterial-associated infection by bactericidal peptide 2. Antimicrob Agents Chemother 2006, 50: 3977–3983. 10.1128/AAC.00575-06PubMedCentralCrossRefPubMed
7.
go back to reference Trampuz A, Piper KE, Jacobson MJ, Hanssen AD, Unni KK, Osmon DR, Mandrekar JN, Cockerill FR, Steckelberg JM, Greenleaf JF, Patel R: Sonication of removed hip and knee prostheses for diagnosis of infection. N Engl J Med 2007, 357: 654–663. 10.1056/NEJMoa061588CrossRefPubMed Trampuz A, Piper KE, Jacobson MJ, Hanssen AD, Unni KK, Osmon DR, Mandrekar JN, Cockerill FR, Steckelberg JM, Greenleaf JF, Patel R: Sonication of removed hip and knee prostheses for diagnosis of infection. N Engl J Med 2007, 357: 654–663. 10.1056/NEJMoa061588CrossRefPubMed
8.
go back to reference Teterycz D, Ferry T, Lew D, Stern R, Assal M, Hoffmeyer P, Bernard L, Uçkay I: Outcome of orthopedic implant infections due to different staphylococci. Int J Infect Dis 2010, 14: e913-e918. 10.1016/j.ijid.2010.05.014CrossRefPubMed Teterycz D, Ferry T, Lew D, Stern R, Assal M, Hoffmeyer P, Bernard L, Uçkay I: Outcome of orthopedic implant infections due to different staphylococci. Int J Infect Dis 2010, 14: e913-e918. 10.1016/j.ijid.2010.05.014CrossRefPubMed
9.
go back to reference Gemmel F, Van den Wyngaert H, Love C, Welling MM, Gemmel P, Palestro CJ: Prosthetic joint infections: radionuclide state-of-the-art imaging. Eur J Nucl Med Mol Imaging 2012, 39: 892–909. 10.1007/s00259-012-2062-7CrossRefPubMed Gemmel F, Van den Wyngaert H, Love C, Welling MM, Gemmel P, Palestro CJ: Prosthetic joint infections: radionuclide state-of-the-art imaging. Eur J Nucl Med Mol Imaging 2012, 39: 892–909. 10.1007/s00259-012-2062-7CrossRefPubMed
10.
go back to reference Glaudemans AW, Galli F, Pacilio M, Signore A: Leukocyte and bacteria imaging in prosthetic joint infection. Eur Cell Mater 2013, 25: 61–77.PubMed Glaudemans AW, Galli F, Pacilio M, Signore A: Leukocyte and bacteria imaging in prosthetic joint infection. Eur Cell Mater 2013, 25: 61–77.PubMed
11.
go back to reference Della Valle C, Parvizi J, Bauer TW, DiCesare PE, Evans RP, Segreti J, Spangehl M, Watters WC 3rd, Keith M, Turkelson CM, Wies JL, Sluka P, Hitchcock K: American Academy of Orthopaedic Surgeons clinical practice guideline on: the diagnosis of periprosthetic joint infections of the hip and knee. J Bone Joint Surg Am 2011, 93: 1355–1357. 10.2106/JBJS.9314eboCrossRefPubMed Della Valle C, Parvizi J, Bauer TW, DiCesare PE, Evans RP, Segreti J, Spangehl M, Watters WC 3rd, Keith M, Turkelson CM, Wies JL, Sluka P, Hitchcock K: American Academy of Orthopaedic Surgeons clinical practice guideline on: the diagnosis of periprosthetic joint infections of the hip and knee. J Bone Joint Surg Am 2011, 93: 1355–1357. 10.2106/JBJS.9314eboCrossRefPubMed
12.
go back to reference Stumpe KD, Nötzli HP, Zanetti M, Kamel EM, Hany TF, Görres GW, von Schulthess GK, Hodler J: FDG PET for differentiation of infection and aseptic loosening in total hip replacements: comparison with conventional radiography and three-phase bone scintigraphy. Radiology 2004, 231: 333–341. 10.1148/radiol.2312021596CrossRefPubMed Stumpe KD, Nötzli HP, Zanetti M, Kamel EM, Hany TF, Görres GW, von Schulthess GK, Hodler J: FDG PET for differentiation of infection and aseptic loosening in total hip replacements: comparison with conventional radiography and three-phase bone scintigraphy. Radiology 2004, 231: 333–341. 10.1148/radiol.2312021596CrossRefPubMed
13.
go back to reference Koort JK, Mäkinen TJ, Knuuti J, Jalava J, Aro HT: Comparative 18 F-FDG PET of experimental Staphylococcus aureus osteomyelitis and normal bone healing. J Nucl Med 2004, 45: 1406–1411.PubMed Koort JK, Mäkinen TJ, Knuuti J, Jalava J, Aro HT: Comparative 18 F-FDG PET of experimental Staphylococcus aureus osteomyelitis and normal bone healing. J Nucl Med 2004, 45: 1406–1411.PubMed
14.
go back to reference Mäkinen TJ, Veiranto M, Knuuti J, Jalava J, Törmälä P, Aro HT: Efficacy of bioabsorbable antibiotic containing bone screw in the prevention of biomaterial-related infection due to Staphylococcus aureus . Bone 2005, 36: 292–299. 10.1016/j.bone.2004.11.009CrossRefPubMed Mäkinen TJ, Veiranto M, Knuuti J, Jalava J, Törmälä P, Aro HT: Efficacy of bioabsorbable antibiotic containing bone screw in the prevention of biomaterial-related infection due to Staphylococcus aureus . Bone 2005, 36: 292–299. 10.1016/j.bone.2004.11.009CrossRefPubMed
15.
go back to reference Koort JK, Mäkinen TJ, Suokas E, Veiranto M, Jalava J, Knuuti J, Törmälä P, Aro HT: Efficacy of ciprofloxacin-releasing bioabsorbable osteoconductive bone defect filler for treatment of experimental osteomyelitis due to Staphylococcus aureus . Antimicrob Agents Chemother 2005, 49: 1502–1508. 10.1128/AAC.49.4.1502-1508.2005PubMedCentralCrossRefPubMed Koort JK, Mäkinen TJ, Suokas E, Veiranto M, Jalava J, Knuuti J, Törmälä P, Aro HT: Efficacy of ciprofloxacin-releasing bioabsorbable osteoconductive bone defect filler for treatment of experimental osteomyelitis due to Staphylococcus aureus . Antimicrob Agents Chemother 2005, 49: 1502–1508. 10.1128/AAC.49.4.1502-1508.2005PubMedCentralCrossRefPubMed
16.
go back to reference Lankinen P, Lehtimäki K, Hakanen AJ, Roivainen A, Aro HT: A comparative 18 F-FDG PET/CT imaging of experimental Staphylococcus aureus osteomyelitis and Staphylococcus epidermidis foreign-body-associated infection in the rabbit tibia. EJNMMI Res 2012, 2: 41. 10.1186/2191-219X-2-41PubMedCentralCrossRefPubMed Lankinen P, Lehtimäki K, Hakanen AJ, Roivainen A, Aro HT: A comparative 18 F-FDG PET/CT imaging of experimental Staphylococcus aureus osteomyelitis and Staphylococcus epidermidis foreign-body-associated infection in the rabbit tibia. EJNMMI Res 2012, 2: 41. 10.1186/2191-219X-2-41PubMedCentralCrossRefPubMed
17.
go back to reference Salmi M, Jalkanen S: A 90-kilodalton endothelial cell molecule mediating lymphocyte binding in humans. Science 1992, 257: 1407–1409. 10.1126/science.1529341CrossRefPubMed Salmi M, Jalkanen S: A 90-kilodalton endothelial cell molecule mediating lymphocyte binding in humans. Science 1992, 257: 1407–1409. 10.1126/science.1529341CrossRefPubMed
18.
go back to reference Jaakkola K, Nikula T, Holopainen R, Vähäsilta T, Matikainen MT, Laukkanen ML, Huupponen R, Halkola L, Nieminen L, Hiltunen J, Parviainen S, Clark MR, Knuuti J, Savunen T, Kääpä P, Voipio-Pulkki LM, Jalkanen S: In vivo detection of vascular adhesion protein-1 in experimental inflammation. Am J Pathol 2000, 157: 463–471. 10.1016/S0002-9440(10)64558-0PubMedCentralCrossRefPubMed Jaakkola K, Nikula T, Holopainen R, Vähäsilta T, Matikainen MT, Laukkanen ML, Huupponen R, Halkola L, Nieminen L, Hiltunen J, Parviainen S, Clark MR, Knuuti J, Savunen T, Kääpä P, Voipio-Pulkki LM, Jalkanen S: In vivo detection of vascular adhesion protein-1 in experimental inflammation. Am J Pathol 2000, 157: 463–471. 10.1016/S0002-9440(10)64558-0PubMedCentralCrossRefPubMed
19.
go back to reference Salmi M, Jalkanen S: VAP-1: an adhesin and an enzyme. Trends Immunol 2001, 22: 211–216. 10.1016/S1471-4906(01)01870-1CrossRefPubMed Salmi M, Jalkanen S: VAP-1: an adhesin and an enzyme. Trends Immunol 2001, 22: 211–216. 10.1016/S1471-4906(01)01870-1CrossRefPubMed
20.
go back to reference Crocker PR, McMillan SJ, Richards HE: CD33-related siglecs as potential modulators of inflammatory responses. Ann N Y Acad Sci 2012, 1253: 102–111. 10.1111/j.1749-6632.2011.06449.xCrossRefPubMed Crocker PR, McMillan SJ, Richards HE: CD33-related siglecs as potential modulators of inflammatory responses. Ann N Y Acad Sci 2012, 1253: 102–111. 10.1111/j.1749-6632.2011.06449.xCrossRefPubMed
21.
go back to reference Aalto K, Autio A, Kiss EA, Elima K, Nymalm Y, Veres TZ, Marttila-Ichihara F, Elovaara H, Saanijoki T, Crocker PR, Maksimow M, Bligt E, Salminen TA, Salmi M, Roivainen A, Jalkanen S: Siglec-9 is a novel leukocyte ligand for vascular adhesion protein-1 and can be used in PET imaging of inflammation and cancer. Blood 2011, 118: 3725–3733. 10.1182/blood-2010-09-311076CrossRefPubMed Aalto K, Autio A, Kiss EA, Elima K, Nymalm Y, Veres TZ, Marttila-Ichihara F, Elovaara H, Saanijoki T, Crocker PR, Maksimow M, Bligt E, Salminen TA, Salmi M, Roivainen A, Jalkanen S: Siglec-9 is a novel leukocyte ligand for vascular adhesion protein-1 and can be used in PET imaging of inflammation and cancer. Blood 2011, 118: 3725–3733. 10.1182/blood-2010-09-311076CrossRefPubMed
22.
go back to reference Merritt JH, Kadouri DE, O'Toole GA: Growing and analyzing static biofilms. Curr Protoc Microbiol 2005, 1: 1B.1. Merritt JH, Kadouri DE, O'Toole GA: Growing and analyzing static biofilms. Curr Protoc Microbiol 2005, 1: 1B.1.
23.
go back to reference Petty W, Spanier S, Shuster JJ, Silverthorne C: The influence of skeletal implants on incidence of infection. Experiments in a canine model. J Bone Joint Surg Am 1985, 67: 1236–1244.PubMed Petty W, Spanier S, Shuster JJ, Silverthorne C: The influence of skeletal implants on incidence of infection. Experiments in a canine model. J Bone Joint Surg Am 1985, 67: 1236–1244.PubMed
24.
go back to reference Rantakokko-Jalava K, Nikkari S, Eerola E, Skurnik M, Meurman O, Ruuskanen O, Alanen A, Kotilainen E, Toivanen P, Kotilainen P: Direct amplification of rRNA genes in diagnosis of bacterial infections. J Clin Microbiol 2000, 38: 32–39.PubMedCentralPubMed Rantakokko-Jalava K, Nikkari S, Eerola E, Skurnik M, Meurman O, Ruuskanen O, Alanen A, Kotilainen E, Toivanen P, Kotilainen P: Direct amplification of rRNA genes in diagnosis of bacterial infections. J Clin Microbiol 2000, 38: 32–39.PubMedCentralPubMed
26.
go back to reference Lankinen P, Mäkinen TJ, Pöyhönen TA, Virsu P, Salomäki S, Hakanen AJ, Jalkanen S, Aro HT, Roivainen A: (68)Ga-DOTAVAP-P1 PET imaging capable of demonstrating the phase of inflammation in healing bones and the progress of infection in osteomyelitic bones. Eur J Nucl Med Mol Imaging 2008, 35: 352–364. 10.1007/s00259-007-0637-5CrossRefPubMed Lankinen P, Mäkinen TJ, Pöyhönen TA, Virsu P, Salomäki S, Hakanen AJ, Jalkanen S, Aro HT, Roivainen A: (68)Ga-DOTAVAP-P1 PET imaging capable of demonstrating the phase of inflammation in healing bones and the progress of infection in osteomyelitic bones. Eur J Nucl Med Mol Imaging 2008, 35: 352–364. 10.1007/s00259-007-0637-5CrossRefPubMed
27.
go back to reference Ujula T, Salomäki S, Virsu P, Lankinen P, Mäkinen TJ, Autio A, Yegutkin GG, Knuuti J, Jalkanen S, Roivainen A: Synthesis, 68Ga labeling and preliminary evaluation of DOTA peptide binding vascular adhesion protein-1: a potential PET imaging agent for diagnosing osteomyelitis. Nucl Med Biol 2009, 36: 631–641. 10.1016/j.nucmedbio.2009.04.008CrossRefPubMed Ujula T, Salomäki S, Virsu P, Lankinen P, Mäkinen TJ, Autio A, Yegutkin GG, Knuuti J, Jalkanen S, Roivainen A: Synthesis, 68Ga labeling and preliminary evaluation of DOTA peptide binding vascular adhesion protein-1: a potential PET imaging agent for diagnosing osteomyelitis. Nucl Med Biol 2009, 36: 631–641. 10.1016/j.nucmedbio.2009.04.008CrossRefPubMed
28.
go back to reference Autio A, Ujula T, Luoto P, Salomäki S, Jalkanen S, Roivainen A: PET imaging of inflammation and adenocarcinoma xenografts using vascular adhesion protein 1 targeting peptide (68)Ga-DOTAVAP-P1: comparison with (18)F-FDG. Eur J Nucl Med Mol Imaging 2010, 37: 1918–1925. 10.1007/s00259-010-1497-yCrossRefPubMed Autio A, Ujula T, Luoto P, Salomäki S, Jalkanen S, Roivainen A: PET imaging of inflammation and adenocarcinoma xenografts using vascular adhesion protein 1 targeting peptide (68)Ga-DOTAVAP-P1: comparison with (18)F-FDG. Eur J Nucl Med Mol Imaging 2010, 37: 1918–1925. 10.1007/s00259-010-1497-yCrossRefPubMed
29.
go back to reference Autio A, Henttinen T, Sipilä HJ, Jalkanen S, Roivainen A: Mini-PEG spacering of VAP-1-targeting 68Ga-DOTAVAP-P1 peptide improves PET imaging of inflammation. EJNMMI Res 2011, 1: 10. 10.1186/2191-219X-1-10PubMedCentralCrossRefPubMed Autio A, Henttinen T, Sipilä HJ, Jalkanen S, Roivainen A: Mini-PEG spacering of VAP-1-targeting 68Ga-DOTAVAP-P1 peptide improves PET imaging of inflammation. EJNMMI Res 2011, 1: 10. 10.1186/2191-219X-1-10PubMedCentralCrossRefPubMed
30.
go back to reference Volk A, Crémieux AC, Belmatoug N, Vallois JM, Pocidalo JJ, Carbon C: Evaluation of a rabbit model for osteomyelitis by high field, high resolution imaging using the chemical-shift-specific-slice-selection technique. Magn Reson Imaging 1994, 12: 1039–1046. 10.1016/0730-725X(94)91235-OCrossRefPubMed Volk A, Crémieux AC, Belmatoug N, Vallois JM, Pocidalo JJ, Carbon C: Evaluation of a rabbit model for osteomyelitis by high field, high resolution imaging using the chemical-shift-specific-slice-selection technique. Magn Reson Imaging 1994, 12: 1039–1046. 10.1016/0730-725X(94)91235-OCrossRefPubMed
31.
go back to reference Crémieux AC, Carbon C: Experimental models of bone and prosthetic joint infections. Clin Infect Dis 1997, 25: 1295–1302. 10.1086/516135CrossRefPubMed Crémieux AC, Carbon C: Experimental models of bone and prosthetic joint infections. Clin Infect Dis 1997, 25: 1295–1302. 10.1086/516135CrossRefPubMed
32.
go back to reference Hienz SA, Sakamoto H, Flock JI, Mörner AC, Reinholt FP, Heimdahl A, Nord CE: Development and characterization of a new model of hematogenous osteomyelitis in the rat. J Infect Dis 1995, 171: 1230–1236. 10.1093/infdis/171.5.1230CrossRefPubMed Hienz SA, Sakamoto H, Flock JI, Mörner AC, Reinholt FP, Heimdahl A, Nord CE: Development and characterization of a new model of hematogenous osteomyelitis in the rat. J Infect Dis 1995, 171: 1230–1236. 10.1093/infdis/171.5.1230CrossRefPubMed
33.
go back to reference Gratz S, Rennen HJ, Boerman OC, Oyen WJ, Burma P, Corstens FH: (99 m)Tc-interleukin-8 for imaging acute osteomyelitis. J Nucl Med 2001, 42: 1257–1264.PubMed Gratz S, Rennen HJ, Boerman OC, Oyen WJ, Burma P, Corstens FH: (99 m)Tc-interleukin-8 for imaging acute osteomyelitis. J Nucl Med 2001, 42: 1257–1264.PubMed
34.
go back to reference Mäkinen TJ, Lankinen P, Pöyhönen T, Jalava J, Aro HT, Roivainen A: Comparison of 18 F-FDG and 68Ga PET imaging in the assessment of experimental osteomyelitis due to Staphylococcus aureus . Eur J Nucl Med Mol Imaging 2005, 32: 1259–1268. 10.1007/s00259-005-1841-9CrossRefPubMed Mäkinen TJ, Lankinen P, Pöyhönen T, Jalava J, Aro HT, Roivainen A: Comparison of 18 F-FDG and 68Ga PET imaging in the assessment of experimental osteomyelitis due to Staphylococcus aureus . Eur J Nucl Med Mol Imaging 2005, 32: 1259–1268. 10.1007/s00259-005-1841-9CrossRefPubMed
35.
go back to reference An YH, Kang QK, Arciola CR: Animal models of osteomyelitis. Int J Artif Organs 2006, 29: 407–420.PubMed An YH, Kang QK, Arciola CR: Animal models of osteomyelitis. Int J Artif Organs 2006, 29: 407–420.PubMed
36.
go back to reference Mayberry-Carson KJ, Tober-Meyer B, Smith JK, Lambe DW Jr, Costerton JW: Bacterial adherence and glycocalyx formation in osteomyelitis experimentally induced with Staphylococcus aureus . Infect Immun 1984, 43: 825–833.PubMedCentralPubMed Mayberry-Carson KJ, Tober-Meyer B, Smith JK, Lambe DW Jr, Costerton JW: Bacterial adherence and glycocalyx formation in osteomyelitis experimentally induced with Staphylococcus aureus . Infect Immun 1984, 43: 825–833.PubMedCentralPubMed
37.
go back to reference Lambe DW Jr, Ferguson KP, Mayberry-Carson KJ, Tober-Meyer B, Costerton JW: Foreign-body-associated experimental osteomyelitis induced with Bacteroides fragilis and Staphylococcus epidermidis in rabbits. Clin Orthop Relat Res 1991, 266: 285–294.PubMed Lambe DW Jr, Ferguson KP, Mayberry-Carson KJ, Tober-Meyer B, Costerton JW: Foreign-body-associated experimental osteomyelitis induced with Bacteroides fragilis and Staphylococcus epidermidis in rabbits. Clin Orthop Relat Res 1991, 266: 285–294.PubMed
38.
go back to reference An YH, Friedman RJ: Animal models of orthopedic implant infection. J Invest Surg 1998, 11: 139–146. 10.3109/08941939809032193CrossRefPubMed An YH, Friedman RJ: Animal models of orthopedic implant infection. J Invest Surg 1998, 11: 139–146. 10.3109/08941939809032193CrossRefPubMed
39.
go back to reference Alt V, Lips KS, Henkenbehrens C, Muhrer D, Oliveira Cavalcanti MC, Sommer U, Thormann U, Szalay G, Heiss C, Pavlidis T, Domann E, Schnettler R: A new animal model for implant-related infected non-unions after intramedullary fixation of the tibia in rats with fluorescent in situ hybridization of bacteria in bone infection. Bone 2011, 48: 1146–1153. 10.1016/j.bone.2011.01.018CrossRefPubMed Alt V, Lips KS, Henkenbehrens C, Muhrer D, Oliveira Cavalcanti MC, Sommer U, Thormann U, Szalay G, Heiss C, Pavlidis T, Domann E, Schnettler R: A new animal model for implant-related infected non-unions after intramedullary fixation of the tibia in rats with fluorescent in situ hybridization of bacteria in bone infection. Bone 2011, 48: 1146–1153. 10.1016/j.bone.2011.01.018CrossRefPubMed
40.
go back to reference Del Pozo JL, Rouse MS, Euba G, Kang CI, Mandrekar JN, Steckelberg JM, Patel R: The electricidal effect is active in an experimental model of Staphylococcus epidermidis chronic foreign body osteomyelitis. Antimicrob Agents Chemother 2009, 53: 4064–4068. 10.1128/AAC.00432-09PubMedCentralCrossRefPubMed Del Pozo JL, Rouse MS, Euba G, Kang CI, Mandrekar JN, Steckelberg JM, Patel R: The electricidal effect is active in an experimental model of Staphylococcus epidermidis chronic foreign body osteomyelitis. Antimicrob Agents Chemother 2009, 53: 4064–4068. 10.1128/AAC.00432-09PubMedCentralCrossRefPubMed
41.
go back to reference Sakaeda H: Experimental polymicrobial osteomyelitis produced by both aerobic and anaerobic opportunistic pathogens. Nihon Seikeigeka Gakkai Zasshi 1988, 62: 791–802.PubMed Sakaeda H: Experimental polymicrobial osteomyelitis produced by both aerobic and anaerobic opportunistic pathogens. Nihon Seikeigeka Gakkai Zasshi 1988, 62: 791–802.PubMed
42.
go back to reference Glaudemans AW, de Vries EF, Vermeulen LE, Slart RH, Dierckx RA, Signore A: A large retrospective single-centre study to define the best image acquisition protocols and interpretation criteria for white blood cell scintigraphy with 99mTc-HMPAO-labelled leucocytes in musculoskeletal infections. Eur J Nucl Med Mol Imaging 2013, 40: 1760–1769. 10.1007/s00259-013-2481-0CrossRefPubMed Glaudemans AW, de Vries EF, Vermeulen LE, Slart RH, Dierckx RA, Signore A: A large retrospective single-centre study to define the best image acquisition protocols and interpretation criteria for white blood cell scintigraphy with 99mTc-HMPAO-labelled leucocytes in musculoskeletal infections. Eur J Nucl Med Mol Imaging 2013, 40: 1760–1769. 10.1007/s00259-013-2481-0CrossRefPubMed
44.
go back to reference Lazzeri E, Israel O, Erba PA, Chakravartty R, Comin JM, Jamar F, Rouzet F, Glaudemans AW, Signore A: Comment on Aksoy et al.: FDG and FDG-labelled leucocyte PET/CT in the imaging of prosthetic joint infection. Eur J Nucl Med Mol Imaging 2014, 41: 1811–1812. 10.1007/s00259-014-2777-8CrossRefPubMed Lazzeri E, Israel O, Erba PA, Chakravartty R, Comin JM, Jamar F, Rouzet F, Glaudemans AW, Signore A: Comment on Aksoy et al.: FDG and FDG-labelled leucocyte PET/CT in the imaging of prosthetic joint infection. Eur J Nucl Med Mol Imaging 2014, 41: 1811–1812. 10.1007/s00259-014-2777-8CrossRefPubMed
45.
go back to reference Love C, Marwin SE, Palestro CJ: Nuclear medicine and the infected joint replacement. Semin Nucl Med 2009, 39: 66–78. 10.1053/j.semnuclmed.2008.08.007CrossRefPubMed Love C, Marwin SE, Palestro CJ: Nuclear medicine and the infected joint replacement. Semin Nucl Med 2009, 39: 66–78. 10.1053/j.semnuclmed.2008.08.007CrossRefPubMed
Metadata
Title
68Ga-DOTA-Siglec-9 PET/CT imaging of peri-implant tissue responses and staphylococcal infections
Authors
Helena Ahtinen
Julia Kulkova
Laura Lindholm
Erkki Eerola
Antti J Hakanen
Niko Moritz
Mirva Söderström
Tiina Saanijoki
Sirpa Jalkanen
Anne Roivainen
Hannu T Aro
Publication date
01-12-2014
Publisher
Springer Berlin Heidelberg
Published in
EJNMMI Research / Issue 1/2014
Electronic ISSN: 2191-219X
DOI
https://doi.org/10.1186/s13550-014-0045-3

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