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Chondrosarcoma

Changed by Joachim Feger, 4 Apr 2023
Back to revision history
Disclosures - updated 26 Nov 2022: Nothing to disclose

Updates to Article Attributes

Body was changed:

Chondrosarcomas are a heterogeneous group of malignant cartilaginous tumours that account for ~25% of all primary malignant bone tumours. They are most commonly found in older patients within the long bones and. They can arise de novo or secondary from an existing benign cartilaginous neoplasm. On On imaging, these tumours have ring-and-arc chondroid matrix mineralisation with aggressive features such as lytic pattern, deep deep endosteal scalloping and soft-tissue extension.

Epidemiology

The typical presentation is inChondrosarcomas account for about 20-25% of all bone tumours and are the 4ththird most common malignant tumour of bone after myeloma and 5osteosarcoma th1,2 decades.

Associations

Some chondrosarcomas originate from precursor lesions namely osteochondromas or enchondromas and there isare associated with the following:

Diagnosis

A provisional diagnosis can be often made by a slight male predominancecombination of clinical information, the location of the tumour and characteristic imaging features. The diagnosis of the exact subtype and tumour grading might require histology and/or molecular pathology 1.5-2:1.

Clinical presentation

Patients usually present with pain, pathological fracture, a palpable lump or a local mass effect. They are also found incidentally in imaging studies. Some chondrosarcomas present with a pathological fracture. 

Hyperglycaemia can occur as a paraneoplastic syndromeref.

Pathology

TheChondrosarcomas are aggressive cartilage matrix-forming tumours and are either primary, arising de novo, or secondary originating from a pre-existent cartilaginous mass 3. Their histology of chondrosarcomas can differ according to their subtype (see below).

In general, thesethe tumours are multilobulated (due to hyaline cartilage nodules) with central high water content and peripheralendochondral ossification. ThisOn imaging, this accounts not only for the high T2 MRI signal (see below) but also forrings and arcs calcification or  or popcorn calcification.

Subtypes

Chondrosarcomas can be clasified into the follwing subtypes:

Grading

Chondrosarcomas are divided into three (sometimes four) grades based primarily on cellularity (see: chondrosarcoma grading).

Subtypes

Chondrosarcomas are either primary, arising de novo, or secondary and arise from a pre-existent cartilaginous mass (see: secondary chondrosarcoma).

Primary
Secondary

Arising from pre-existing cartilaginous lesions:

DistributionLocation

  • long bones: 45% (the reason is that the cartilage is more abundant in the long, tubular bones)

  • pelvis: 25% especially around the triradiate cartilage

  • ribs: 8%

    • patients often younger than at other sites

    • anterior ribs/costochondral junction

  • spine: 7%

    • greater male predominance 2-4:1

    • thoracic most common

    • location

      • posterior elements and vertebral body 45%

      • posterior elements only 40%

      • vertebral body only 15%

  • scapula: 5%

  • sternum: 2%

  • head and neck (including cervical spine): 6-7%

  • craniofacial: 2% (see chondrosarcoma of the skull base)

  • hands and feet: rare cf. enchondromas

Radiographic features

Imaging findings vary somewhat with different subtypes but do have some general features. Below are typical imaging appearances which are best demonstrated by conventional chondrosarcomas.

In general chondrosarcomas are large masses at the time of diagnosis, usually >4 cm in diameter and >10 cm in 50% of cases.

Plain radiograph
CT

The features seen on CT are the same as on plain film, but are simply better seen:

  • 94% of cases demonstrate matrix calcification, cf. 60-78% on plain film

  • endosteal scalloping

  • cortical breach, seen in ~90% of long bone chondrosarcoma, cf. only ~10% of enchondromas

  • soft tissue mass: tumour cellularity, and therefore density, increases with the increased grade of the tumour

  • heterogenous contrast enhancement

MRI

  • T1: low to intermediate signal

    • iso- to slightly hyperintense cf. muscle

    • iso- to slightly hypointense cf. grey matter (see chondrosarcoma of the base of the skull)

  • T2: very high intensity in non-mineralised/calcified portions - the cartilage is a hydrophilic tissue with high water content6

  • gradient echo/SWI: blooming of mineralised/calcified portions

  • T1 C+ (Gd) 

    • enhancement can be septal and peripheral rim-like corresponding to fibrovascular septation between lobules of hyaline cartilage - rings and arcs enhancement pattern6,7

    • most demonstrate heterogeneous moderate to intense contrast enhancement.

Nuclear medicine

Typically chondrosarcomas demonstrate increased uptake on bone scan, seen in over 80% of cases, and usually, the uptake is quite intense. This is useful in helping to distinguish low-grade chondrosarcoma from an enchondroma as the latter has increased uptake in ~20% of cases, and usually to a lesser degree (see: enchondroma vs low grade-grade chondrosarcoma).

Treatment and prognosis

Prognosis variesThe management and prognosis depend on the subtype, the histological grade and the location of the tumours (see also respective articles). Treatment usually involves surgery, and the type of excision will again vary with boththe type, grade and location of the tumour 2. In general:Chemotherapy and radiation generally play no role, except for mesenchymal chondrosarcomas2,3.

  • grade

    • grade 1: 90% 5-year survival

    • grade 3: 29% 5-year survival

  • location

    • long bones have a better prognosis than axial skeleton
  • -<p><strong>Chondrosarcomas</strong> are malignant cartilaginous tumours that account for ~25% of all <a href="/articles/primary-malignant-bone-tumours">primary malignant bone tumours</a>. They are most commonly found in older patients within the long bones and can arise de novo or secondary from an existing benign cartilaginous neoplasm. On imaging, these tumours have ring-and-arc chondroid matrix mineralisation with aggressive features such as lytic pattern, deep endosteal scalloping and soft-tissue extension.</p><h4>Epidemiology</h4><p>The typical presentation is in the 4<sup>th</sup> and 5<sup>th</sup> decades and there is a slight male predominance of 1.5-2:1.</p><h4>Clinical presentation</h4><p>Patients usually present with pain, pathological fracture, a palpable lump or local mass effect. <a href="/articles/hyperglycaemia">Hyperglycaemia</a> can occur as a <a href="/articles/paraneoplastic-syndromes">paraneoplastic syndrome</a>.</p><h4>Pathology</h4><p>The histology of chondrosarcomas can differ according to their subtype (see below). In general, these tumours are multilobulated (due to hyaline cartilage nodules) with central high water content and peripheral <a href="/articles/endochondral-ossification">endochondral ossification</a>. This accounts not only for the high T2 MRI signal (see below) but also for <a href="/articles/rings-and-arcs-calcification">rings and arcs calcification</a> or <a href="/articles/popcorn-calcification-disambiguation">popcorn calcification</a>.</p><h5>Grading</h5><p>Chondrosarcomas are divided into three (sometimes four) grades based primarily on cellularity (see: <a href="/articles/chondrosarcoma-grading">chondrosarcoma grading</a>).</p><h5>Subtypes</h5><p>Chondrosarcomas are either primary, arising de novo, or secondary and arise from a pre-existent cartilaginous mass (see: <a href="/articles/secondary-chondrosarcoma">secondary chondrosarcoma</a>).</p><h6>Primary</h6><ul>
  • -<li><p><a href="/articles/conventional-intramedullary-chondrosarcoma">conventional intramedullary chondrosarcoma</a> (or central chondrosarcoma): low, intermediate or high grade (see: <a href="/articles/chondrosarcoma-grading">chondrosarcoma grading</a>)</p></li>
  • -<li><p><a href="/articles/periosteal-chondrosarcoma-1">juxtacortical chondrosarcoma</a>: low, intermediate or high grade</p></li>
  • -<li><p><a href="/articles/clear-cell-chondrosarcoma">clear cell chondrosarcoma</a></p></li>
  • -<li><p><a href="/articles/myxoid-chondrosarcoma">myxoid chondrosarcoma</a>: usually intermediate grade</p></li>
  • -<li><p><a href="/articles/mesenchymal-chondrosarcoma">mesenchymal chondrosarcoma</a>: usually high grade</p></li>
  • -<li><p><a href="/articles/extraskeletal-chondrosarcoma">extraskeletal chondrosarcoma</a></p></li>
  • -<li><p><a href="/articles/dedifferentiated-chondrosarcoma">dedifferentiated chondrosarcoma</a></p></li>
  • -</ul><h6>Secondary</h6><p>Arising from pre-existing cartilaginous lesions:</p><ul>
  • -<li>
  • -<p><a href="/articles/osteochondroma">osteochondroma</a></p>
  • -<ul>
  • -<li><p>solitary osteochondroma</p></li>
  • -<li><p><a href="/articles/hereditary-multiple-exostoses">hereditary multiple exostoses</a></p></li>
  • -</ul>
  • -</li>
  • -<li>
  • -<p><a href="/articles/enchondroma">enchondroma</a></p>
  • -<ul>
  • -<li><p>solitary enchondroma</p></li>
  • +<p><strong>Chondrosarcomas</strong> are a heterogeneous group of malignant cartilaginous tumours most commonly found in older patients. They can arise de novo or secondary from an existing benign cartilaginous neoplasm. On imaging, these tumours have ring-and-arc chondroid matrix mineralisation with aggressive features such as lytic pattern, deep endosteal scalloping and soft-tissue extension.</p><h4>Epidemiology</h4><p>Chondrosarcomas account for about 20-25% of all bone tumours and are the third most common malignant tumour of bone after myeloma and osteosarcoma <sup>1,2</sup>.</p><h5>Associations</h5><p>Some chondrosarcomas originate from precursor lesions namely <a href="/articles/osteochondroma" title="Osteochondromas">osteochondromas</a> or <a href="/articles/enchondroma" title="Enchondromas">enchondromas</a> and are associated with the following:</p><ul>
  • +<li><p>solitary <a href="/articles/osteochondroma" title="Osteochondromas">osteochondromas</a> and <a href="/articles/hereditary-multiple-exostoses" title="Hereditary multiple exostoses">hereditary multiple exostoses</a></p></li>
  • -</ul>
  • -</li>
  • -</ul><h5>Distribution</h5><ul><li>
  • +</ul><h4>Diagnosis</h4><p>A provisional diagnosis can be often made by a combination of clinical information, the location of the tumour and characteristic imaging features. The diagnosis of the exact subtype and tumour grading might require histology and/or molecular pathology <sup>1</sup>.</p><h4>Clinical presentation</h4><p>Patients usually present with pain, a palpable lump or a local mass effect. They are also found incidentally in imaging studies. Some chondrosarcomas present with a <a href="/articles/pathological-fracture" title="Pathological fracture">pathological fracture</a>. </p><p><a href="/articles/hyperglycaemia">Hyperglycaemia</a> can occur as a <a href="/articles/paraneoplastic-syndromes">paraneoplastic syndrome</a> <sup>ref</sup>.</p><h4>Pathology</h4><p>Chondrosarcomas are aggressive cartilage matrix-forming tumours and are either primary, arising de novo, or secondary originating from a pre-existent cartilaginous mass <sup>3</sup>. Their histology can differ according to their subtype (see below).</p><p>In general, the tumours are multilobulated (due to hyaline cartilage nodules) with central high water content and peripheral <a href="/articles/endochondral-ossification">endochondral ossification</a>. On imaging, this accounts not only for the high T2 MRI signal (see below) but also for <a href="/articles/rings-and-arcs-calcification">rings and arcs calcification</a> or <a href="/articles/popcorn-calcification-disambiguation">popcorn calcification</a>.</p><h5>Subtypes</h5><p>Chondrosarcomas can be clasified into the follwing subtypes:</p><ul>
  • +<li>
  • +<p><a href="/articles/conventional-chondrosarcoma" title="Conventional chondrosarcoma">conventional chondrosarcoma</a> (85-90%) <sup>1,4</sup></p>
  • +<ul>
  • +<li><p><a href="/articles/central-atypical-cartilaginous-tumour-low-grade-chondrosarcoma" title="Central atypical cartilaginous tumour/low-grade chondrosarcoma">central atypical cartilaginous tumours/chondrosarcoma grade 1 (ACT/CS1)</a></p></li>
  • +<li><p><a href="/articles/central-intermediate-and-high-grade-chondrosarcoma" title="Central chondrosarcomas grade 2 and 3 (CS2/CS3)">central chondrosarcomas grades 2 and 3</a></p></li>
  • +<li><p><a href="/articles/peripheral-atypical-cartilaginous-tumour-low-grade-peripheral-chondrosarcoma-1" title="Secondary peripheral atypical cartilaginous tumour">secondary peripheral atypical cartilaginous tumours/chondrosarcomas grade 1 (ACT/CS1)</a></p></li>
  • +<li><p><a href="/articles/peripheral-intermediate-and-high-grade-chondrosarcoma" title="Secondary peripheral chondrosarcoma grade 2 and 3">secondary peripheral chondrosarcomas grades 2 and 3</a></p></li>
  • +</ul>
  • +</li>
  • +<li><p><a href="/articles/dedifferentiated-chondrosarcoma">dedifferentiated chondrosarcoma</a> (in up to 10% of conventional carcinomas) <sup>3</sup></p></li>
  • +<li><p><a href="/articles/mesenchymal-chondrosarcoma">mesenchymal chondrosarcoma</a> (~2-4%) <sup>3</sup></p></li>
  • +<li><p><a href="/articles/periosteal-chondrosarcoma-1">periosteal chondrosarcoma</a> (~2-3%) <sup>3</sup></p></li>
  • +<li><p><a href="/articles/clear-cell-chondrosarcoma">clear cell chondrosarcoma</a> (~2%)</p></li>
  • +<li><p><a href="/articles/extraskeletal-chondrosarcoma-1" title="Extraskeletal chondrosarcoma">extraskeletal chondrosarcoma</a> (~1%)</p></li>
  • +</ul><h5>Grading</h5><p>Chondrosarcomas are divided into three (sometimes four) grades based primarily on cellularity (see: <a href="/articles/chondrosarcoma-grading">chondrosarcoma grading</a>).</p><h5>Location</h5><ul><li>
  • -</ul><h5>CT</h5><p>The features seen on CT are the same as on plain film, but are simply better seen:</p><ul>
  • +</ul><h5>CT</h5><p>The features seen on CT are the same as on plain film but are simply better seen:</p><ul>
  • -<li><p>soft tissue mass: tumour cellularity, and therefore density, increases with increased grade of the tumour</p></li>
  • +<li><p>soft tissue mass: tumour cellularity, and therefore density, increases with the increased grade of the tumour</p></li>
  • -<li><p>iso- to slightly hypointense cf. grey matter (see chondrosarcoma of the base of skull)</p></li>
  • +<li><p>iso- to slightly hypointense cf. grey matter (see chondrosarcoma of the base of the skull)</p></li>
  • -</ul><h5>Nuclear medicine</h5><p>Typically chondrosarcomas demonstrate increased uptake on <a href="/articles/bone-scintigraphy-1">bone scan</a>, seen in over 80% of cases, and usually the uptake is quite intense. This is useful in helping to distinguish low-grade chondrosarcoma from an enchondroma as the latter has increased uptake in ~20% of cases, and usually to a lesser degree (see: <a href="/articles/enchondroma-vs-low-grade-chondrosarcoma-3">enchondroma vs low grade chondrosarcoma</a>).</p><h4>Treatment and prognosis</h4><p>Prognosis varies with both grade and location. In general:</p><ul>
  • -<li>
  • -<p>grade</p>
  • -<ul>
  • -<li><p>grade 1: 90% 5-year survival</p></li>
  • -<li><p>grade 3: 29% 5-year survival</p></li>
  • -</ul>
  • -</li>
  • -<li>
  • -<p>location</p>
  • -<ul><li><p>long bones have a better prognosis than axial skeleton</p></li></ul>
  • -</li>
  • -</ul>
  • +</ul><h5>Nuclear medicine</h5><p>Typically chondrosarcomas demonstrate increased uptake on <a href="/articles/bone-scintigraphy-1">bone scan</a>, seen in over 80% of cases, and usually, the uptake is quite intense. This is useful in helping to distinguish low-grade chondrosarcoma from an enchondroma as the latter has increased uptake in ~20% of cases, and usually to a lesser degree (see: <a href="/articles/enchondroma-vs-low-grade-chondrosarcoma-3">enchondroma vs low-grade chondrosarcoma</a>).</p><h4>Treatment and prognosis</h4><p>The management and prognosis depend on the subtype, the histological grade and the location of the tumours (see also respective articles). Treatment usually involves surgery, and the type of excision will again vary with the type, grade and location of the tumour <sup>2</sup>. Chemotherapy and radiation generally play no role, except for <a href="/articles/mesenchymal-chondrosarcoma" title="Mesenchymal chondrosarcomas (MCS)">mesenchymal chondrosarcomas</a> <sup>2,3</sup>. </p>

References changed:

  • 1. Murphey M, Walker E, Wilson A, Kransdorf M, Temple H, Gannon F. From the Archives of the AFIP: Imaging of Primary Chondrosarcoma: Radiologic-Pathologic Correlation. Radiographics. 2003;23(5):1245-78. <a href="https://doi.org/10.1148/rg.235035134">doi:10.1148/rg.235035134</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/12975513">Pubmed</a>
  • 2. Gelderblom H, Hogendoorn P, Dijkstra S et al. The Clinical Approach Towards Chondrosarcoma. Oncologist. 2008;13(3):320-9. <a href="https://doi.org/10.1634/theoncologist.2007-0237">doi:10.1634/theoncologist.2007-0237</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/18378543">Pubmed</a>
  • 4. van Praag Veroniek V, Rueten-Budde A, Ho V et al. Incidence, Outcomes and Prognostic Factors During 25 Years of Treatment of Chondrosarcomas. Surg Oncol. 2018;27(3):402-8. <a href="https://doi.org/10.1016/j.suronc.2018.05.009">doi:10.1016/j.suronc.2018.05.009</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/30217294">Pubmed</a>
  • 4. van Praag Veroniek V, Rueten-Budde A, Ho V et al. Incidence, Outcomes and Prognostic Factors During 25 Years of Treatment of Chondrosarcomas. Surg Oncol. 2018;27(3):402-8. <a href="https://doi.org/10.1016/j.suronc.2018.05.009">doi:10.1016/j.suronc.2018.05.009</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/30217294">Pubmed</a>
  • 3. WHO Classification of Tumours Editorial Board. Soft tissue and bone tumours. Lyon (France): International Agency for Research on Cancer; 2020. (WHO classification of tumours series, 5th ed.; vol. 3). <a href="https://publications.iarc.fr/Book-And-Report-Series/Who-Classification-Of-Tumours/Soft-Tissue-And-Bone-Tumours-2020">https://publications.iarc.fr</a>
  • 3. WHO Classification of Tumours Editorial Board. Soft tissue and bone tumours. Lyon (France): International Agency for Research on Cancer; 2020. (WHO classification of tumours series, 5th ed.; vol. 3). <a href="https://publications.iarc.fr/Book-And-Report-Series/Who-Classification-Of-Tumours/Soft-Tissue-And-Bone-Tumours-2020">https://publications.iarc.fr</a>
  • 6. Meyers S, Hirsch W, Curtin H, Barnes L, Sekhar L, Sen C. Chondrosarcomas of the Skull Base: MR Imaging Features. Radiology. 1992;184(1):103-8. <a href="https://doi.org/10.1148/radiology.184.1.1609064">doi:10.1148/radiology.184.1.1609064</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/1609064">Pubmed</a>
  • 5. Varma D, Ayala A, Carrasco C, Guo S, Kumar R, Edeiken J. Chondrosarcoma: MR Imaging with Pathologic Correlation. Radiographics. 1992;12(4):687-704. <a href="https://doi.org/10.1148/radiographics.12.4.1636034">doi:10.1148/radiographics.12.4.1636034</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/1636034">Pubmed</a>
  • 7. Geirnaerdt M, Hogendoorn P, Bloem J, Taminiau A, van der Woude H. Cartilaginous Tumors: Fast Contrast-Enhanced MR Imaging. Radiology. 2000;214(2):539-46. <a href="https://doi.org/10.1148/radiology.214.2.r00fe12539">doi:10.1148/radiology.214.2.r00fe12539</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/10671608">Pubmed</a>
  • 8. Engel H, Herget G, Füllgraf H et al. Chondrogenic Bone Tumors: The Importance of Imaging Characteristics. Rofo. 2021;193(3):262-75. <a href="https://doi.org/10.1055/a-1288-1209">doi:10.1055/a-1288-1209</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/33152784">Pubmed</a>
  • 9. Aoki J, Sone S, Fujioka F et al. MR of Enchondroma and Chondrosarcoma: Rings and Arcs of Gd-DTPA Enhancement. J Comput Assist Tomogr. 1991;15(6):1011-6. <a href="https://doi.org/10.1097/00004728-199111000-00021">doi:10.1097/00004728-199111000-00021</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/1939751">Pubmed</a>
  • 1. Wolfgang Dähnert. Radiology Review Manual. (2003) ISBN: 9780781738958 - <a href="http://books.google.com/books?vid=ISBN9780781738958">Google Books</a>
  • 4. Murphey M, Walker E, Wilson A, Kransdorf M, Temple H, Gannon F. From the Archives of the AFIP: Imaging of Primary Chondrosarcoma: Radiologic-Pathologic Correlation. Radiographics. 2003;23(5):1245-78. <a href="https://doi.org/10.1148/rg.235035134">doi:10.1148/rg.235035134</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/12975513">Pubmed</a>
  • 3. van Praag Veroniek V, Rueten-Budde A, Ho V et al. Incidence, Outcomes and Prognostic Factors During 25 Years of Treatment of Chondrosarcomas. Surg Oncol. 2018;27(3):402-8. <a href="https://doi.org/10.1016/j.suronc.2018.05.009">doi:10.1016/j.suronc.2018.05.009</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/30217294">Pubmed</a>
  • 4. WHO Classification of Tumours Editorial Board. Soft tissue and bone tumours. Lyon (France): International Agency for Research on Cancer; 2020. (WHO classification of tumours series, 5th ed.; vol. 3). <a href="https://publications.iarc.fr/Book-And-Report-Series/Who-Classification-Of-Tumours/Soft-Tissue-And-Bone-Tumours-2020">https://publications.iarc.fr</a>
  • 2. Meyers S, Hirsch W, Curtin H, Barnes L, Sekhar L, Sen C. Chondrosarcomas of the Skull Base: MR Imaging Features. Radiology. 1992;184(1):103-8. <a href="https://doi.org/10.1148/radiology.184.1.1609064">doi:10.1148/radiology.184.1.1609064</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/1609064">Pubmed</a>
  • 3. Varma D, Ayala A, Carrasco C, Guo S, Kumar R, Edeiken J. Chondrosarcoma: MR Imaging with Pathologic Correlation. Radiographics. 1992;12(4):687-704. <a href="https://doi.org/10.1148/radiographics.12.4.1636034">doi:10.1148/radiographics.12.4.1636034</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/1636034">Pubmed</a>
  • 5. Geirnaerdt M, Hogendoorn P, Bloem J, Taminiau A, van der Woude H. Cartilaginous Tumors: Fast Contrast-Enhanced MR Imaging. Radiology. 2000;214(2):539-46. <a href="https://doi.org/10.1148/radiology.214.2.r00fe12539">doi:10.1148/radiology.214.2.r00fe12539</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/10671608">Pubmed</a>
  • 6. Engel H, Herget G, Füllgraf H et al. Chondrogenic Bone Tumors: The Importance of Imaging Characteristics. Rofo. 2021;193(3):262-75. <a href="https://doi.org/10.1055/a-1288-1209">doi:10.1055/a-1288-1209</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/33152784">Pubmed</a>
  • 7. Aoki J, Sone S, Fujioka F et al. MR of Enchondroma and Chondrosarcoma: Rings and Arcs of Gd-DTPA Enhancement. J Comput Assist Tomogr. 1991;15(6):1011-6. <a href="https://doi.org/10.1097/00004728-199111000-00021">doi:10.1097/00004728-199111000-00021</a> - <a href="https://www.ncbi.nlm.nih.gov/pubmed/1939751">Pubmed</a>

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