Skip to main content
Top
Published in: Skeletal Radiology 3/2015

01-03-2015 | Review Article

Periosteum: Characteristic imaging findings with emphasis on radiologic-pathologic comparisons

Authors: Damien Bisseret, Rachid Kaci, Marie-Hélène Lafage-Proust, Marianne Alison, Caroline Parlier-Cuau, Jean-Denis Laredo, Valérie Bousson

Published in: Skeletal Radiology | Issue 3/2015

Login to get access

Abstract

The periosteum covers most bone structures. It has an outer fibrous layer and an inner cambial layer that exhibits osteogenic activity. The periosteum is a dynamic structure that plays a major role in bone modeling and remodeling under normal conditions. In several disorders such as infections, benign and malignant tumors, and systemic diseases, the osteogenic potential of the periosteum is stimulated and new bone is produced. The newly formed bone added onto the surface of the cortex adopts various configurations depending on the modalities and pace of bone production. Our aim here is to describe the anatomy, histology, and physiology of the periosteum and to review the various patterns of periosteal reaction with emphasis on relations between radiological and histopathological findings. A careful evaluation of the periosteal reaction and appearance of the underlying cortex, in combination with the MRI, clinical, and laboratory data, provides valuable information on lesion duration and aggressiveness, thereby assisting in the etiological diagnosis and optimizing patient management. A solid reaction strongly suggests a benign and slow-growing process that gives the bone enough time to wall off the lesion. Single lamellar reactions occur in acute and usually benign diseases. Multilamellar reactions are associated with intermediate aggressiveness and a growth rate close to the limit of the walling-off capabilities of the bone. Spiculated, interrupted, and complex combined reactions carry the worst prognosis, as they occur in the most aggressive and fast-growing diseases: the periosteum attempts to create new bone but is overwhelmed and may be breached.
Literature
2.
go back to reference Rauch F. Bone growth in length and width: the Yin and Yang of bone stability. J Musculoskelet Neuronal Interact. 2005;5(3):194–201.PubMed Rauch F. Bone growth in length and width: the Yin and Yang of bone stability. J Musculoskelet Neuronal Interact. 2005;5(3):194–201.PubMed
3.
go back to reference Orwoll ES. Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res. 2003;18(6):949–54.PubMedCrossRef Orwoll ES. Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res. 2003;18(6):949–54.PubMedCrossRef
4.
go back to reference Zhang X, Awad HA, O’Keefe RJ, Guldberg RE, Schwarz EM. A perspective: engineering periosteum for structural bone graft healing. Clin Orthop Relat Res. 2008;466(8):1777–87.PubMedCentralPubMedCrossRef Zhang X, Awad HA, O’Keefe RJ, Guldberg RE, Schwarz EM. A perspective: engineering periosteum for structural bone graft healing. Clin Orthop Relat Res. 2008;466(8):1777–87.PubMedCentralPubMedCrossRef
5.
go back to reference Allen MR, Hock JM, Burr DB. Periosteum: biology, regulation, and response to osteoporosis therapies. Bone. 2004;35(5):1003–12.PubMedCrossRef Allen MR, Hock JM, Burr DB. Periosteum: biology, regulation, and response to osteoporosis therapies. Bone. 2004;35(5):1003–12.PubMedCrossRef
6.
go back to reference Ragsdale BD, Madewell JE, Sweet DE. Radiologic and pathologic analysis of solitary bone lesions. Part II: periosteal reactions. Radiol Clin North Am. 1981;19(4):749–83.PubMed Ragsdale BD, Madewell JE, Sweet DE. Radiologic and pathologic analysis of solitary bone lesions. Part II: periosteal reactions. Radiol Clin North Am. 1981;19(4):749–83.PubMed
7.
go back to reference Mills SE, editor. Histology for pathologists. 4th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2012. Mills SE, editor. Histology for pathologists. 4th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2012.
8.
go back to reference Klein MJ. Non-Neoplastic Diseases of Bones and Joints: Atlas of Nontumor Pathology. American Registry of Pathology; 2011. Klein MJ. Non-Neoplastic Diseases of Bones and Joints: Atlas of Nontumor Pathology. American Registry of Pathology; 2011.
9.
go back to reference Hill EL, Elde R. Distribution of CGRP-, VIP-, D beta H-, SP-, and NPY-immunoreactive nerves in the periosteum of the rat. Cell Tissue Res. 1991;264(3):469–80.PubMedCrossRef Hill EL, Elde R. Distribution of CGRP-, VIP-, D beta H-, SP-, and NPY-immunoreactive nerves in the periosteum of the rat. Cell Tissue Res. 1991;264(3):469–80.PubMedCrossRef
10.
go back to reference Hohmann EL, Elde RP, Rysavy JA, Einzig S, Gebhard RL. Innervation of periosteum and bone by sympathetic vasoactive intestinal peptide-containing nerve fibers. Science. 1986;232(4752):868–71.PubMedCrossRef Hohmann EL, Elde RP, Rysavy JA, Einzig S, Gebhard RL. Innervation of periosteum and bone by sympathetic vasoactive intestinal peptide-containing nerve fibers. Science. 1986;232(4752):868–71.PubMedCrossRef
11.
go back to reference Mach DB, Rogers SD, Sabino MC, Luger NM, Schwei MJ, Pomonis JD, et al. Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroscience. 2002;113(1):155–66.PubMedCrossRef Mach DB, Rogers SD, Sabino MC, Luger NM, Schwei MJ, Pomonis JD, et al. Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroscience. 2002;113(1):155–66.PubMedCrossRef
12.
go back to reference Tonna EA. Response of the cellular phase of the skeleton to trauma. Periodontics. 1966;4(3):105–14.PubMed Tonna EA. Response of the cellular phase of the skeleton to trauma. Periodontics. 1966;4(3):105–14.PubMed
13.
go back to reference Tang XM, Chai BF. Ultrastructural investigation of osteogenic cells. Chin Med J. 1986;99(12):950–6.PubMed Tang XM, Chai BF. Ultrastructural investigation of osteogenic cells. Chin Med J. 1986;99(12):950–6.PubMed
14.
15.
go back to reference Ito Y, Fitzsimmons JS, Sanyal A, Mello MA, Mukherjee N, O’Driscoll SW. Localization of chondrocyte precursors in periosteum. Osteoarthr Cartil. 2001;9(3):215–23.PubMedCrossRef Ito Y, Fitzsimmons JS, Sanyal A, Mello MA, Mukherjee N, O’Driscoll SW. Localization of chondrocyte precursors in periosteum. Osteoarthr Cartil. 2001;9(3):215–23.PubMedCrossRef
16.
go back to reference Diaz-Flores L, Gutierrez R, Lopez-Alonso A, Gonzalez R, Varela H. Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis. Clin Orthop Relat Res. 1992;275:280–6.PubMed Diaz-Flores L, Gutierrez R, Lopez-Alonso A, Gonzalez R, Varela H. Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis. Clin Orthop Relat Res. 1992;275:280–6.PubMed
17.
go back to reference Duhamel H. Cited by Bassett CAL in current concepts of bone formation. J Bone Joint Surg. 1739;44-A:1217–44. Duhamel H. Cited by Bassett CAL in current concepts of bone formation. J Bone Joint Surg. 1739;44-A:1217–44.
18.
go back to reference Ollier L. Traité expérimentale et clinique de la régénération des os et de la production artificielle du tissu osseux. Paris: Masson et Fils; 1867. Ollier L. Traité expérimentale et clinique de la régénération des os et de la production artificielle du tissu osseux. Paris: Masson et Fils; 1867.
19.
go back to reference Jacobsen FS. Periosteum: its relation to pediatric fractures. J Pediatr Orthop B. 1997;6(2):84–90.PubMedCrossRef Jacobsen FS. Periosteum: its relation to pediatric fractures. J Pediatr Orthop B. 1997;6(2):84–90.PubMedCrossRef
20.
go back to reference Szulc P, Seeman E, Duboeuf F, Sornay-Rendu E, Delmas PD. Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res. 2006;21(12):1856–63.PubMedCrossRef Szulc P, Seeman E, Duboeuf F, Sornay-Rendu E, Delmas PD. Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res. 2006;21(12):1856–63.PubMedCrossRef
21.
go back to reference Seeman E. Periosteal bone formation–a neglected determinant of bone strength. N Engl J Med. 2003;349(4):320–3.PubMedCrossRef Seeman E. Periosteal bone formation–a neglected determinant of bone strength. N Engl J Med. 2003;349(4):320–3.PubMedCrossRef
22.
go back to reference Kim B-T, Mosekilde L, Duan Y, Zhang X-Z, Tornvig L, Thomsen JS, et al. The structural and hormonal basis of sex differences in peak appendicular bone strength in rats. J Bone Miner Res. 2003;18(1):150–5.PubMedCrossRef Kim B-T, Mosekilde L, Duan Y, Zhang X-Z, Tornvig L, Thomsen JS, et al. The structural and hormonal basis of sex differences in peak appendicular bone strength in rats. J Bone Miner Res. 2003;18(1):150–5.PubMedCrossRef
23.
go back to reference Turner RT, Wakley GK, Hannon KS. Differential effects of androgens on cortical bone histomorphometry in gonadectomized male and female rats. J Orthop Res. 1990;8(4):612–7.PubMedCrossRef Turner RT, Wakley GK, Hannon KS. Differential effects of androgens on cortical bone histomorphometry in gonadectomized male and female rats. J Orthop Res. 1990;8(4):612–7.PubMedCrossRef
24.
go back to reference Parfitt AM. Parathyroid hormone and periosteal bone expansion. J Bone Miner Res. 2002;17(10):1741–3.PubMedCrossRef Parfitt AM. Parathyroid hormone and periosteal bone expansion. J Bone Miner Res. 2002;17(10):1741–3.PubMedCrossRef
25.
go back to reference Dempster DW, Cosman F, Kurland ES, Zhou H, Nieves J, Woelfert L, et al. Effects of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis: a paired biopsy study. J Bone Miner Res. 2001;16(10):1846–53.PubMedCrossRef Dempster DW, Cosman F, Kurland ES, Zhou H, Nieves J, Woelfert L, et al. Effects of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis: a paired biopsy study. J Bone Miner Res. 2001;16(10):1846–53.PubMedCrossRef
26.
go back to reference Jiang Y, Zhao JJ, Mitlak BH, Wang O, Genant HK, Eriksen EF. Recombinant human parathyroid hormone (1-34) [teriparatide] improves both cortical and cancellous bone structure. J Bone Miner Res. 2003;18(11):1932–41.PubMedCrossRef Jiang Y, Zhao JJ, Mitlak BH, Wang O, Genant HK, Eriksen EF. Recombinant human parathyroid hormone (1-34) [teriparatide] improves both cortical and cancellous bone structure. J Bone Miner Res. 2003;18(11):1932–41.PubMedCrossRef
27.
go back to reference Ma YL, Zeng Q, Donley DW, Ste-Marie L-G, Gallagher JC, Dalsky GP, et al. Teriparatide increases bone formation in modeling and remodeling osteons and enhances IGF-II immunoreactivity in postmenopausal women with osteoporosis. J Bone Miner Res. 2006;21(6):855–64.PubMedCrossRef Ma YL, Zeng Q, Donley DW, Ste-Marie L-G, Gallagher JC, Dalsky GP, et al. Teriparatide increases bone formation in modeling and remodeling osteons and enhances IGF-II immunoreactivity in postmenopausal women with osteoporosis. J Bone Miner Res. 2006;21(6):855–64.PubMedCrossRef
28.
go back to reference Specker B, Binkley T. Randomized trial of physical activity and calcium supplementation on bone mineral content in 3- to 5-year-old children. J Bone Miner Res. 2003;18(5):885–92.PubMedCrossRef Specker B, Binkley T. Randomized trial of physical activity and calcium supplementation on bone mineral content in 3- to 5-year-old children. J Bone Miner Res. 2003;18(5):885–92.PubMedCrossRef
29.
go back to reference Zhu K, Greenfield H, Du X, Zhang Q, Fraser DR. Effects of milk supplementation on cortical bone gain in Chinese girls aged 10-12 years. Asia Pac J Clin Nutr. 2003;12:S47. Zhu K, Greenfield H, Du X, Zhang Q, Fraser DR. Effects of milk supplementation on cortical bone gain in Chinese girls aged 10-12 years. Asia Pac J Clin Nutr. 2003;12:S47.
30.
go back to reference McKenzie JA, Silva MJ. Comparing histological, vascular and molecular responses associated with woven and lamellar bone formation induced by mechanical loading in the rat ulna. Bone. 2011;48(2):250–8.PubMedCentralPubMedCrossRef McKenzie JA, Silva MJ. Comparing histological, vascular and molecular responses associated with woven and lamellar bone formation induced by mechanical loading in the rat ulna. Bone. 2011;48(2):250–8.PubMedCentralPubMedCrossRef
31.
go back to reference Feik SA, Ellender G, Crowe DM, Ramm-Anderson SM. Periosteal response in translation-induced bone remodelling. J Anat. 1990;171:69–84.PubMedCentralPubMed Feik SA, Ellender G, Crowe DM, Ramm-Anderson SM. Periosteal response in translation-induced bone remodelling. J Anat. 1990;171:69–84.PubMedCentralPubMed
32.
go back to reference Frost HM, Schönau E. The “muscle-bone unit” in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab. 2000;13(6):571–90.PubMedCrossRef Frost HM, Schönau E. The “muscle-bone unit” in children and adolescents: a 2000 overview. J Pediatr Endocrinol Metab. 2000;13(6):571–90.PubMedCrossRef
33.
go back to reference Hamrick MW, McNeil PL, Patterson SL. Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact. 2010;10(1):64–70.PubMedCentralPubMed Hamrick MW, McNeil PL, Patterson SL. Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact. 2010;10(1):64–70.PubMedCentralPubMed
34.
go back to reference Elkasrawy MN, Hamrick MW. Myostatin (GDF-8) as a key factor linking muscle mass and bone structure. J Musculoskelet Neuronal Interact. 2010;10(1):56–63.PubMedCentralPubMed Elkasrawy MN, Hamrick MW. Myostatin (GDF-8) as a key factor linking muscle mass and bone structure. J Musculoskelet Neuronal Interact. 2010;10(1):56–63.PubMedCentralPubMed
36.
go back to reference Kenan S, Abdelwahab IF, Klein MJ, Hermann G, Lewis MM. Lesions of juxtacortical origin (surface lesions of bone). Skeletal Radiol. 1993;22(5):337–57.PubMedCrossRef Kenan S, Abdelwahab IF, Klein MJ, Hermann G, Lewis MM. Lesions of juxtacortical origin (surface lesions of bone). Skeletal Radiol. 1993;22(5):337–57.PubMedCrossRef
37.
go back to reference Wenaden AET, Szyszko TA, Saifuddin A. Imaging of periosteal reactions associated with focal lesions of bone. Clin Radiol. 2005;60(4):439–56.PubMedCrossRef Wenaden AET, Szyszko TA, Saifuddin A. Imaging of periosteal reactions associated with focal lesions of bone. Clin Radiol. 2005;60(4):439–56.PubMedCrossRef
38.
39.
go back to reference Miller TT. Bone tumors and tumorlike conditions: analysis with conventional radiography. Radiology. 2008;246(3):662–74.PubMedCrossRef Miller TT. Bone tumors and tumorlike conditions: analysis with conventional radiography. Radiology. 2008;246(3):662–74.PubMedCrossRef
40.
go back to reference Ballikar R, Balikar R, Redkar NN, Patil MA, Pillai R. Hair-on-end appearance in a case of thalassemia intermedia. BMJ Case Rep. 2013;2013. Ballikar R, Balikar R, Redkar NN, Patil MA, Pillai R. Hair-on-end appearance in a case of thalassemia intermedia. BMJ Case Rep. 2013;2013.
41.
go back to reference Bastug D, Ortiz O, Schochet SS. Hemangiomas in the calvaria: imaging findings. AJR Am J Roentgenol. 1995;164(3):683–7.PubMedCrossRef Bastug D, Ortiz O, Schochet SS. Hemangiomas in the calvaria: imaging findings. AJR Am J Roentgenol. 1995;164(3):683–7.PubMedCrossRef
42.
go back to reference Kim KS, Rogers LF, Goldblatt D. CT features of hyperostosing meningioma en plaque. AJR Am J Roentgenol. 1987;149(5):1017–23.PubMedCrossRef Kim KS, Rogers LF, Goldblatt D. CT features of hyperostosing meningioma en plaque. AJR Am J Roentgenol. 1987;149(5):1017–23.PubMedCrossRef
43.
go back to reference Sundaram M, McGuire MH. Computed tomography or magnetic resonance for evaluating the solitary tumor or tumor-like lesion of bone? Skeletal Radiol. 1988;17(6):393–401.PubMedCrossRef Sundaram M, McGuire MH. Computed tomography or magnetic resonance for evaluating the solitary tumor or tumor-like lesion of bone? Skeletal Radiol. 1988;17(6):393–401.PubMedCrossRef
44.
go back to reference Magid D. Two-dimensional and three-dimensional computed tomographic imaging in musculoskeletal tumors. Radiol Clin North Am. 1993;31(2):425–47.PubMed Magid D. Two-dimensional and three-dimensional computed tomographic imaging in musculoskeletal tumors. Radiol Clin North Am. 1993;31(2):425–47.PubMed
45.
go back to reference Greenfield GB, Warren DL, Clark RA. MR imaging of periosteal and cortical changes of bone. Radiographics. 1991;11(4):611–23. discussion 624.PubMedCrossRef Greenfield GB, Warren DL, Clark RA. MR imaging of periosteal and cortical changes of bone. Radiographics. 1991;11(4):611–23. discussion 624.PubMedCrossRef
46.
go back to reference Dosdá R, Martí-Bonmatí L, Menor F, Aparisi F, Rodrigo C, Ricart V. Comparison of plain radiographs and magnetic resonance images in the evaluation of periosteal reaction and osteoid matrix in osteosarcomas. MAGMA. 1999;9(1–2):72–80.PubMedCrossRef Dosdá R, Martí-Bonmatí L, Menor F, Aparisi F, Rodrigo C, Ricart V. Comparison of plain radiographs and magnetic resonance images in the evaluation of periosteal reaction and osteoid matrix in osteosarcomas. MAGMA. 1999;9(1–2):72–80.PubMedCrossRef
47.
go back to reference Spaeth HJ, Chandnani VP, Beltran J, Lucas JG, Ortiz I, King MA, et al. Magnetic resonance imaging detection of early experimental periostitis. Comparison of magnetic resonance imaging, computed tomography, and plain radiography with histopathologic correlation. Invest Radiol. 1991;26(4):304–8.PubMedCrossRef Spaeth HJ, Chandnani VP, Beltran J, Lucas JG, Ortiz I, King MA, et al. Magnetic resonance imaging detection of early experimental periostitis. Comparison of magnetic resonance imaging, computed tomography, and plain radiography with histopathologic correlation. Invest Radiol. 1991;26(4):304–8.PubMedCrossRef
48.
go back to reference Bloem JL, Taminiau AH, Eulderink F, Hermans J, Pauwels EK. Radiologic staging of primary bone sarcoma: MR imaging, scintigraphy, angiography, and CT correlated with pathologic examination. Radiology. 1988;169(3):805–10.PubMedCrossRef Bloem JL, Taminiau AH, Eulderink F, Hermans J, Pauwels EK. Radiologic staging of primary bone sarcoma: MR imaging, scintigraphy, angiography, and CT correlated with pathologic examination. Radiology. 1988;169(3):805–10.PubMedCrossRef
49.
go back to reference Frouge C, Vanel D, Coffre C, Couanet D, Contesso G, Sarrazin D. The role of magnetic resonance imaging in the evaluation of Ewing sarcoma. A report of 27 cases. Skeletal Radiol. 1988;17(6):387–92.PubMedCrossRef Frouge C, Vanel D, Coffre C, Couanet D, Contesso G, Sarrazin D. The role of magnetic resonance imaging in the evaluation of Ewing sarcoma. A report of 27 cases. Skeletal Radiol. 1988;17(6):387–92.PubMedCrossRef
50.
go back to reference Saifuddin A. The accuracy of imaging in the local staging of appendicular osteosarcoma. Skeletal Radiol. 2002;31(4):191–201.PubMedCrossRef Saifuddin A. The accuracy of imaging in the local staging of appendicular osteosarcoma. Skeletal Radiol. 2002;31(4):191–201.PubMedCrossRef
51.
go back to reference Saifuddin A, Burnett SJ, Mitchell R. Pictorial review: ultrasonography of primary bone tumours. Clin Radiol. 1998;53(4):239–46.PubMedCrossRef Saifuddin A, Burnett SJ, Mitchell R. Pictorial review: ultrasonography of primary bone tumours. Clin Radiol. 1998;53(4):239–46.PubMedCrossRef
52.
go back to reference Bilkay U, Tokat C, Helvaci E, Ozek C, Zekioglu O, Onat T, et al. Osteogenic capacities of tibial and cranial periosteum: a biochemical and histologic study. J Craniofac Surg. 2008;19(2):453–8.PubMedCrossRef Bilkay U, Tokat C, Helvaci E, Ozek C, Zekioglu O, Onat T, et al. Osteogenic capacities of tibial and cranial periosteum: a biochemical and histologic study. J Craniofac Surg. 2008;19(2):453–8.PubMedCrossRef
53.
go back to reference Lodwick G. A systematic approach to the roentgen diagnosis of bone tumors. Tumors of bone and soft tissue. M.D. Anderson Hospital and Tumor Institute, Chicago; 1965. p. 49–68. Lodwick G. A systematic approach to the roentgen diagnosis of bone tumors. Tumors of bone and soft tissue. M.D. Anderson Hospital and Tumor Institute, Chicago; 1965. p. 49–68.
54.
go back to reference Lodwick GS, Wilson AJ, Farrell C, Virtama P, Dittrich F. Determining growth rates of focal lesions of bone from radiographs. Radiology. 1980;134(3):577–83.PubMedCrossRef Lodwick GS, Wilson AJ, Farrell C, Virtama P, Dittrich F. Determining growth rates of focal lesions of bone from radiographs. Radiology. 1980;134(3):577–83.PubMedCrossRef
55.
go back to reference Madewell JE, Ragsdale BD, Sweet DE. Radiologic and pathologic analysis of solitary bone lesions. Part I: internal margins. Radiol Clin North Am. 1981;19(4):715–48.PubMed Madewell JE, Ragsdale BD, Sweet DE. Radiologic and pathologic analysis of solitary bone lesions. Part I: internal margins. Radiol Clin North Am. 1981;19(4):715–48.PubMed
Metadata
Title
Periosteum: Characteristic imaging findings with emphasis on radiologic-pathologic comparisons
Authors
Damien Bisseret
Rachid Kaci
Marie-Hélène Lafage-Proust
Marianne Alison
Caroline Parlier-Cuau
Jean-Denis Laredo
Valérie Bousson
Publication date
01-03-2015
Publisher
Springer Berlin Heidelberg
Published in
Skeletal Radiology / Issue 3/2015
Print ISSN: 0364-2348
Electronic ISSN: 1432-2161
DOI
https://doi.org/10.1007/s00256-014-1976-5

Other articles of this Issue 3/2015

Skeletal Radiology 3/2015 Go to the issue