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Published in: European Radiology 10/2013

01-10-2013 | Musculoskeletal

Efficacy of intra-tendinous injection of platelet-rich plasma in treating tendinosis: comprehensive assessment of a rat model

Authors: Benjamin Dallaudière, Marta Lempicki, Lionel Pesquer, Liliane Louedec, Pierre Marie Preux, Philippe Meyer, Vincent Hummel, Ahmed Larbi, Lydia Deschamps, Clement Journe, Agathe Hess, Alain Silvestre, Paul Sargos, Philippe Loriaut, Patrick Boyer, Elisabeth Schouman-Claeys, Jean Baptiste Michel, Jean Michel Serfaty

Published in: European Radiology | Issue 10/2013

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Abstract

Objectives

To assess the potential of intra-tendinous injection of platelet rich plasma (PRP) to treat tendinosis (T+) in a rat model of patellar and Achilles T+, and evaluate its local toxicity.

Methods

Thirty rats (120 patellar and Achilles tendons) were used. We induced T+ into 80 tendons (patellar = 40, Achilles = 40) by injecting collagenase at day 0 under ultrasound (US) guidance. Clinical examination and US at day 3, followed by US-guided intra-tendinous injection of either PRP (PRPT+, n = 40) or physiological serum (ST+, n = 40, control). Follow-up was at days 6, 13, 18 and 25 using clinical, US and histological evaluation. To study PRP toxicity, we injected PRP into 40 normal tendons (PRPT-) and compared with 40 untreated normal tendons (T-).

Results

All PRPT+ showed better joint mobilisation compared with ST+ at day 6 (P = 0.005), day 13 (P = 0.02), day 18 (P = 0.003) and day 25 (P = 0.01). Similar results were found regarding US and histology, with smaller collagen fibre diameters (day 6, P = 0.003, day 25, P ≤ 0.004), less disorganisation and fewer neovessels (day 6, P = 0.003, day 25, P = 0.0003) in PRPT+ compared with ST+. Comparison between PRPT- and T- showed no PRP toxicity (P = 0.18).

Conclusions

Our study suggests that mono-injection of PRP in T+ improves tendon healing, with no local toxicity.

Key Points

• We assessed the potential of platelet rich plasma (PRP) to treat tendinosis.
• We treated patellar and Achilles tendinosis in a rat model.
• We evaluated clinical, imaging and histological data.
• Intra-tendinous PRP injection could be useful in the treatment of tendinosis.
Literature
1.
go back to reference Goel DP, Chan D, Watson K, Mohtadi N (2009) Safety and hospital costs of Achilles tendon surgery: the serendipitous impact of a randomized clinical trial. Can J Surg 52:467–472PubMed Goel DP, Chan D, Watson K, Mohtadi N (2009) Safety and hospital costs of Achilles tendon surgery: the serendipitous impact of a randomized clinical trial. Can J Surg 52:467–472PubMed
2.
go back to reference Paavola M, Kannus P, Järvinen TAH et al (2002) Achilles tendinopathy. J Bone Joint Surg Am 84-A:2062–2076PubMed Paavola M, Kannus P, Järvinen TAH et al (2002) Achilles tendinopathy. J Bone Joint Surg Am 84-A:2062–2076PubMed
3.
go back to reference Aström M, Rausing A (1995) Chronic Achilles tendinopathy. A survey of surgical and histopathologic findings. Clin Orthop Relat Res 316:151–164 Aström M, Rausing A (1995) Chronic Achilles tendinopathy. A survey of surgical and histopathologic findings. Clin Orthop Relat Res 316:151–164
4.
go back to reference Khan KM, Maffulli N (1998) Tendinopathy: an Achilles’ heel for athletes and clinicians. Clin J Sport Med 8:151–154PubMedCrossRef Khan KM, Maffulli N (1998) Tendinopathy: an Achilles’ heel for athletes and clinicians. Clin J Sport Med 8:151–154PubMedCrossRef
5.
go back to reference Virchenko O, Fahlgren A, Rundgren M, Aspenberg P (2008) Early Achilles tendon healing in sheep. Arch Orthop Trauma Surg 128:1001–1006PubMedCrossRef Virchenko O, Fahlgren A, Rundgren M, Aspenberg P (2008) Early Achilles tendon healing in sheep. Arch Orthop Trauma Surg 128:1001–1006PubMedCrossRef
6.
go back to reference de Vos RJ, Weir A, Tol JL et al (2011) No effects of PRP on ultrasonographic tendon structure and neovascularisation in chronic midportion Achilles tendinopathy. Br J Sports Med 45:387–392PubMedCrossRef de Vos RJ, Weir A, Tol JL et al (2011) No effects of PRP on ultrasonographic tendon structure and neovascularisation in chronic midportion Achilles tendinopathy. Br J Sports Med 45:387–392PubMedCrossRef
7.
go back to reference Clancy WG Jr, Neidhart D, Brand RL (1976) Achilles tendonitis in runners: a report of five cases. Am J Sports Med 4:46–57PubMedCrossRef Clancy WG Jr, Neidhart D, Brand RL (1976) Achilles tendonitis in runners: a report of five cases. Am J Sports Med 4:46–57PubMedCrossRef
8.
go back to reference Nelen G, Martens M, Burssens A (1989) Surgical treatment of chronic Achilles tendinitis. Am J Sports Med 17:754–759PubMedCrossRef Nelen G, Martens M, Burssens A (1989) Surgical treatment of chronic Achilles tendinitis. Am J Sports Med 17:754–759PubMedCrossRef
10.
go back to reference Clancy WG (1980) Runners’ injuries. Part two. Evaluation and treatment of specific injuries. Am J Sports Med 8:287–289PubMedCrossRef Clancy WG (1980) Runners’ injuries. Part two. Evaluation and treatment of specific injuries. Am J Sports Med 8:287–289PubMedCrossRef
11.
go back to reference Housner JA, Jacobson JA, Misko R (2009) Sonographically guided percutaneous needle tenotomy for the treatment of chronic tendinosis. J Ultrasound Med 28:1187–1192PubMed Housner JA, Jacobson JA, Misko R (2009) Sonographically guided percutaneous needle tenotomy for the treatment of chronic tendinosis. J Ultrasound Med 28:1187–1192PubMed
12.
go back to reference Housner JA, Jacobson JA, Morag Y et al (2010) Should ultrasound-guided needle fenestration be considered as a treatment option for recalcitrant patellar tendinopathy? A retrospective study of 47 cases. Clin J Sport Med 20:488–490PubMedCrossRef Housner JA, Jacobson JA, Morag Y et al (2010) Should ultrasound-guided needle fenestration be considered as a treatment option for recalcitrant patellar tendinopathy? A retrospective study of 47 cases. Clin J Sport Med 20:488–490PubMedCrossRef
13.
go back to reference McShane JM, Nazarian LN, Harwood MI (2006) Sonographically guided percutaneous needle tenotomy for treatment of common extensor tendinosis in the elbow. J Ultrasound Med 25:1281–1289PubMed McShane JM, Nazarian LN, Harwood MI (2006) Sonographically guided percutaneous needle tenotomy for treatment of common extensor tendinosis in the elbow. J Ultrasound Med 25:1281–1289PubMed
14.
go back to reference Rabago D, Best TM, Zgierska AE et al (2009) A systematic review of four injection therapies for lateral epicondylosis: prolotherapy, polidocanol, whole blood and platelet-rich plasma. Br J Sports Med 43:471–481PubMedCrossRef Rabago D, Best TM, Zgierska AE et al (2009) A systematic review of four injection therapies for lateral epicondylosis: prolotherapy, polidocanol, whole blood and platelet-rich plasma. Br J Sports Med 43:471–481PubMedCrossRef
15.
go back to reference Park E-J, Kim E-S, Weber H-P et al (2008) Improved bone healing by angiogenic factor-enriched platelet-rich plasma and its synergistic enhancement by bone morphogenetic protein-2. Int J Oral Maxillofac Implants 23:818–826PubMed Park E-J, Kim E-S, Weber H-P et al (2008) Improved bone healing by angiogenic factor-enriched platelet-rich plasma and its synergistic enhancement by bone morphogenetic protein-2. Int J Oral Maxillofac Implants 23:818–826PubMed
16.
go back to reference De Jonge S, De Vos RJ, Weir A et al (2011) One-year follow-up of platelet-rich plasma treatment in chronic Achilles tendinopathy: a double-blind randomized placebo-controlled trial. Am J Sports Med 39:1623–1629PubMedCrossRef De Jonge S, De Vos RJ, Weir A et al (2011) One-year follow-up of platelet-rich plasma treatment in chronic Achilles tendinopathy: a double-blind randomized placebo-controlled trial. Am J Sports Med 39:1623–1629PubMedCrossRef
17.
go back to reference Del Buono A, Papalia R, Denaro V et al (2011) Platelet rich plasma and tendinopathy: state of the art. Int J Immunopathol Pharmacol 24:79–83PubMed Del Buono A, Papalia R, Denaro V et al (2011) Platelet rich plasma and tendinopathy: state of the art. Int J Immunopathol Pharmacol 24:79–83PubMed
19.
go back to reference Finnoff JT, Fowler SP, Lai JK et al (2011) Treatment of chronic tendinopathy with ultrasound-guided needle tenotomy and platelet-rich plasma injection. PM R 3:900–911PubMedCrossRef Finnoff JT, Fowler SP, Lai JK et al (2011) Treatment of chronic tendinopathy with ultrasound-guided needle tenotomy and platelet-rich plasma injection. PM R 3:900–911PubMedCrossRef
20.
go back to reference Gaweda K, Tarczynska M, Krzyzanowski W (2010) Treatment of Achilles tendinopathy with platelet-rich plasma. Int J Sports Med 31:577–583PubMedCrossRef Gaweda K, Tarczynska M, Krzyzanowski W (2010) Treatment of Achilles tendinopathy with platelet-rich plasma. Int J Sports Med 31:577–583PubMedCrossRef
21.
go back to reference Lee KS, Wilson JJ, Rabago DP et al (2011) Musculoskeletal applications of platelet-rich plasma: fad or future? AJR Am J Roentgenol 196:628–636PubMedCrossRef Lee KS, Wilson JJ, Rabago DP et al (2011) Musculoskeletal applications of platelet-rich plasma: fad or future? AJR Am J Roentgenol 196:628–636PubMedCrossRef
22.
go back to reference Owens RF Jr, Ginnetti J, Conti SF, Latona C (2011) Clinical and magnetic resonance imaging outcomes following platelet rich plasma injection for chronic midsubstance Achilles tendinopathy. Foot Ankle Int 32:1032–1039PubMedCrossRef Owens RF Jr, Ginnetti J, Conti SF, Latona C (2011) Clinical and magnetic resonance imaging outcomes following platelet rich plasma injection for chronic midsubstance Achilles tendinopathy. Foot Ankle Int 32:1032–1039PubMedCrossRef
23.
go back to reference Peerbooms JC, Sluimer J, Bruijn DJ, Gosens T (2010) Positive effect of an autologous platelet concentrate in lateral epicondylitis in a double-blind randomized controlled trial: platelet-rich plasma versus corticosteroid injection with a 1-year follow-up. Am J Sports Med 38:255–262PubMedCrossRef Peerbooms JC, Sluimer J, Bruijn DJ, Gosens T (2010) Positive effect of an autologous platelet concentrate in lateral epicondylitis in a double-blind randomized controlled trial: platelet-rich plasma versus corticosteroid injection with a 1-year follow-up. Am J Sports Med 38:255–262PubMedCrossRef
24.
go back to reference Kader D, Saxena A, Movin T, Maffulli N (2002) Achilles tendinopathy: some aspects of basic science and clinical management. Br J Sports Med 36:239–249PubMedCrossRef Kader D, Saxena A, Movin T, Maffulli N (2002) Achilles tendinopathy: some aspects of basic science and clinical management. Br J Sports Med 36:239–249PubMedCrossRef
25.
go back to reference Coombes BK, Bisset L, Vicenzino B (2010) Efficacy and safety of corticosteroid injections and other injections for management of tendinopathy: a systematic review of randomised controlled trials. Lancet 376:1751–1767PubMedCrossRef Coombes BK, Bisset L, Vicenzino B (2010) Efficacy and safety of corticosteroid injections and other injections for management of tendinopathy: a systematic review of randomised controlled trials. Lancet 376:1751–1767PubMedCrossRef
26.
go back to reference Hart L (2011) Corticosteroid and other injections in the management of tendinopathies: a review. Clin J Sport Med 21:540–541PubMedCrossRef Hart L (2011) Corticosteroid and other injections in the management of tendinopathies: a review. Clin J Sport Med 21:540–541PubMedCrossRef
27.
go back to reference Thanasas C, Papadimitriou G, Charalambidis C et al (2011) Platelet-rich plasma versus autologous whole blood for the treatment of chronic lateral elbow epicondylitis: a randomized controlled clinical trial. Am J Sports Med 39:2130–2134PubMedCrossRef Thanasas C, Papadimitriou G, Charalambidis C et al (2011) Platelet-rich plasma versus autologous whole blood for the treatment of chronic lateral elbow epicondylitis: a randomized controlled clinical trial. Am J Sports Med 39:2130–2134PubMedCrossRef
28.
go back to reference Tohidnezhad M, Varoga D, Wruck CJ et al (2011) Platelet-released growth factors can accelerate tenocyte proliferation and activate the anti-oxidant response element. Histochem Cell Biol 135:453–460PubMedCrossRef Tohidnezhad M, Varoga D, Wruck CJ et al (2011) Platelet-released growth factors can accelerate tenocyte proliferation and activate the anti-oxidant response element. Histochem Cell Biol 135:453–460PubMedCrossRef
29.
go back to reference Van Ark M, Zwerver J, Van den Akker-Scheek I (2011) Injection treatments for patellar tendinopathy. Br J Sports Med 45:1068–1076PubMedCrossRef Van Ark M, Zwerver J, Van den Akker-Scheek I (2011) Injection treatments for patellar tendinopathy. Br J Sports Med 45:1068–1076PubMedCrossRef
30.
go back to reference Carofino B, Chowaniec DM, McCarthy MB et al (2012) Corticosteroids and local anesthetics decrease positive effects of platelet-rich plasma: an in vitro study on human tendon cells. Arthroscopy 28:711–719PubMedCrossRef Carofino B, Chowaniec DM, McCarthy MB et al (2012) Corticosteroids and local anesthetics decrease positive effects of platelet-rich plasma: an in vitro study on human tendon cells. Arthroscopy 28:711–719PubMedCrossRef
31.
go back to reference Geburek F, Stadler P (2011) Regenerative therapy for tendon and ligament disorders in horses. Terminology, production, biologic potential and in vitro effects. Tierarztl Prax Ausg G Grosstiere Nutztiere 39:373–383PubMed Geburek F, Stadler P (2011) Regenerative therapy for tendon and ligament disorders in horses. Terminology, production, biologic potential and in vitro effects. Tierarztl Prax Ausg G Grosstiere Nutztiere 39:373–383PubMed
32.
go back to reference Jo CH, Kim JE, Yoon KS, Shin S (2012) Platelet-rich plasma stimulates cell proliferation and enhances matrix gene expression and synthesis in tenocytes from human rotator cuff tendons with degenerative tears. Am J Sports Med 40:1035–1045PubMedCrossRef Jo CH, Kim JE, Yoon KS, Shin S (2012) Platelet-rich plasma stimulates cell proliferation and enhances matrix gene expression and synthesis in tenocytes from human rotator cuff tendons with degenerative tears. Am J Sports Med 40:1035–1045PubMedCrossRef
33.
go back to reference Kaux J-F, Drion P, Libertiaux V et al (2013) Eccentric training improves tendon biomechanical properties: a rat model. J Orthop Res 31:119–124PubMedCrossRef Kaux J-F, Drion P, Libertiaux V et al (2013) Eccentric training improves tendon biomechanical properties: a rat model. J Orthop Res 31:119–124PubMedCrossRef
34.
go back to reference Kaux J-F, Drion PV, Colige A et al (2012) Effects of platelet-rich plasma (PRP) on the healing of Achilles tendons of rats. Wound Repair Regen 20:748–756PubMedCrossRef Kaux J-F, Drion PV, Colige A et al (2012) Effects of platelet-rich plasma (PRP) on the healing of Achilles tendons of rats. Wound Repair Regen 20:748–756PubMedCrossRef
35.
go back to reference Martinello T, Bronzini I, Perazzi A et al (2013) Effects of in vivo applications of peripheral blood-derived mesenchymal stromal cells (PB-MSCs) and platlet-rich plasma (PRP) on experimentally injured deep digital flexor tendons of sheep. J Orthop Res 31:306–314PubMedCrossRef Martinello T, Bronzini I, Perazzi A et al (2013) Effects of in vivo applications of peripheral blood-derived mesenchymal stromal cells (PB-MSCs) and platlet-rich plasma (PRP) on experimentally injured deep digital flexor tendons of sheep. J Orthop Res 31:306–314PubMedCrossRef
36.
go back to reference Chen L, Dong S-W, Liu J-P et al (2012) Synergy of tendon stem cells and platelet-rich plasma in tendon healing. J Orthop Res 30:991–997PubMedCrossRef Chen L, Dong S-W, Liu J-P et al (2012) Synergy of tendon stem cells and platelet-rich plasma in tendon healing. J Orthop Res 30:991–997PubMedCrossRef
37.
go back to reference De Vos RJ, Van Veldhoven PLJ, Moen MH et al (2010) Autologous growth factor injections in chronic tendinopathy: a systematic review. Br Med Bull 95:63–77PubMedCrossRef De Vos RJ, Van Veldhoven PLJ, Moen MH et al (2010) Autologous growth factor injections in chronic tendinopathy: a systematic review. Br Med Bull 95:63–77PubMedCrossRef
38.
go back to reference Murawski CD, Kennedy JG (2010) Platelet-rich plasma releasate promotes differentiation of tendon stem cells into active tenocytes (Letter to the editor). Am J Sports Med 38:NP3PubMedCrossRef Murawski CD, Kennedy JG (2010) Platelet-rich plasma releasate promotes differentiation of tendon stem cells into active tenocytes (Letter to the editor). Am J Sports Med 38:NP3PubMedCrossRef
40.
go back to reference Zargar Baboldashti N, Poulsen RC, Franklin SL et al (2011) Platelet-rich plasma protects tenocytes from adverse side effects of dexamethasone and ciprofloxacin. Am J Sports Med 39:1929–1935PubMedCrossRef Zargar Baboldashti N, Poulsen RC, Franklin SL et al (2011) Platelet-rich plasma protects tenocytes from adverse side effects of dexamethasone and ciprofloxacin. Am J Sports Med 39:1929–1935PubMedCrossRef
41.
go back to reference Lyras D, Kazakos K, Verettas D et al (2010) Immunohistochemical study of angiogenesis after local administration of platelet-rich plasma in a patellar tendon defect. Int Orthop 34:143–148PubMedCrossRef Lyras D, Kazakos K, Verettas D et al (2010) Immunohistochemical study of angiogenesis after local administration of platelet-rich plasma in a patellar tendon defect. Int Orthop 34:143–148PubMedCrossRef
42.
go back to reference Atik OS (2012) Is the evidence behind platelet-rich plasma therapies strong enough? Eklem Hastalik Cerrahisi 23:1PubMed Atik OS (2012) Is the evidence behind platelet-rich plasma therapies strong enough? Eklem Hastalik Cerrahisi 23:1PubMed
43.
go back to reference Hoksrud AF, Bahr R (2011) Injectable agents derived from or targeting vascularity: has clinical acceptance in managing tendon disorders superseded scientific evidence? J Musculoskelet Neuronal Interact 11:174–184PubMed Hoksrud AF, Bahr R (2011) Injectable agents derived from or targeting vascularity: has clinical acceptance in managing tendon disorders superseded scientific evidence? J Musculoskelet Neuronal Interact 11:174–184PubMed
44.
go back to reference Kampa RJ, Connell DA (2010) Treatment of tendinopathy: is there a role for autologous whole blood and platelet rich plasma injection? Int J Clin Pract 64:1813–1823PubMedCrossRef Kampa RJ, Connell DA (2010) Treatment of tendinopathy: is there a role for autologous whole blood and platelet rich plasma injection? Int J Clin Pract 64:1813–1823PubMedCrossRef
45.
go back to reference Lake SP, Ansorge HL, Soslowsky LJ (2008) Animal models of tendinopathy. Disabil Rehabil 30:1530–1541PubMedCrossRef Lake SP, Ansorge HL, Soslowsky LJ (2008) Animal models of tendinopathy. Disabil Rehabil 30:1530–1541PubMedCrossRef
46.
go back to reference Dragoo JL, Braun HJ, Durham JL et al (2012) Comparison of the acute inflammatory response of two commercial platelet-rich plasma systems in healthy rabbit tendons. Am J Sports Med 40:1274–1281PubMedCrossRef Dragoo JL, Braun HJ, Durham JL et al (2012) Comparison of the acute inflammatory response of two commercial platelet-rich plasma systems in healthy rabbit tendons. Am J Sports Med 40:1274–1281PubMedCrossRef
47.
go back to reference McCarrel TM, Minas T, Fortier LA (2012) Optimization of leukocyte concentration in platelet-rich plasma for the treatment of tendinopathy. J Bone Joint Surg Am 94(19):e143(1–8) McCarrel TM, Minas T, Fortier LA (2012) Optimization of leukocyte concentration in platelet-rich plasma for the treatment of tendinopathy. J Bone Joint Surg Am 94(19):e143(1–8)
48.
go back to reference Schramme M, Hunter S, Campbell N et al (2010) A surgical tendonitis model in horses: technique, clinical, ultrasonographic and histological characterisation. Vet Comp Orthop Traumatol 23:231–239PubMedCrossRef Schramme M, Hunter S, Campbell N et al (2010) A surgical tendonitis model in horses: technique, clinical, ultrasonographic and histological characterisation. Vet Comp Orthop Traumatol 23:231–239PubMedCrossRef
49.
50.
go back to reference Maffulli N, Longo UG, Franceschi F et al (2008) Movin and Bonar scores assess the same characteristics of tendon histology. Clin Orthop Relat Res 466:1605–1611PubMedCrossRef Maffulli N, Longo UG, Franceschi F et al (2008) Movin and Bonar scores assess the same characteristics of tendon histology. Clin Orthop Relat Res 466:1605–1611PubMedCrossRef
51.
go back to reference Foster TE, Puskas BL, Mandelbaum BR et al (2009) Platelet-rich plasma: from basic science to clinical applications. Am J Sports Med 37:2259–2272PubMedCrossRef Foster TE, Puskas BL, Mandelbaum BR et al (2009) Platelet-rich plasma: from basic science to clinical applications. Am J Sports Med 37:2259–2272PubMedCrossRef
52.
go back to reference Alfredson H, Lorentzon M, Bäckman S et al (2003) cDNA-arrays and real-time quantitative PCR techniques in the investigation of chronic Achilles tendinosis. J Orthop Res 21:970–975PubMedCrossRef Alfredson H, Lorentzon M, Bäckman S et al (2003) cDNA-arrays and real-time quantitative PCR techniques in the investigation of chronic Achilles tendinosis. J Orthop Res 21:970–975PubMedCrossRef
53.
go back to reference Buttery LD, Evans TJ, Springall DR et al (1994) Immunochemical localization of inducible nitric oxide synthase in endotoxin-treated rats. Lab Invest 71:755–764PubMed Buttery LD, Evans TJ, Springall DR et al (1994) Immunochemical localization of inducible nitric oxide synthase in endotoxin-treated rats. Lab Invest 71:755–764PubMed
54.
go back to reference Vu TH, Werb Z (2000) Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 14:2123–2133PubMedCrossRef Vu TH, Werb Z (2000) Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 14:2123–2133PubMedCrossRef
55.
go back to reference Sharma P, Maffulli N (2005) Tendon injury and tendinopathy: healing and repair. J Bone Joint Surg Am 87:187–202PubMedCrossRef Sharma P, Maffulli N (2005) Tendon injury and tendinopathy: healing and repair. J Bone Joint Surg Am 87:187–202PubMedCrossRef
Metadata
Title
Efficacy of intra-tendinous injection of platelet-rich plasma in treating tendinosis: comprehensive assessment of a rat model
Authors
Benjamin Dallaudière
Marta Lempicki
Lionel Pesquer
Liliane Louedec
Pierre Marie Preux
Philippe Meyer
Vincent Hummel
Ahmed Larbi
Lydia Deschamps
Clement Journe
Agathe Hess
Alain Silvestre
Paul Sargos
Philippe Loriaut
Patrick Boyer
Elisabeth Schouman-Claeys
Jean Baptiste Michel
Jean Michel Serfaty
Publication date
01-10-2013
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 10/2013
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-013-2926-7

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