70
Views
4
CrossRef citations to date
0
Altmetric
Review

The genetics of osteoarthritis

Pages 503-516 | Published online: 10 Jan 2014

References

  • Heberden W. Commentaries on the history and Cure of Disease, Second Edition. T Payne, London, USA (1803).
  • Haygarth J. A Clinical History of Diseases. Cadell and Davies, London, UK, 147–168 (1805).
  • Stecher RM, Hersh AH. Heberden’s nodes: the mechanism of inheritance in hypertrophic arthritis of the fingers. J. Clin. Invest.23(5), 699–704 (1944).
  • Kellgren JH, Moore R. Generalized osteoarthritis and Heberden’s nodes. Br. Med. J.1(4751), 181–187 (1952).
  • Allison AC, Blumberg BS. Familial osteoarthropathy of the fingers. J. Bone Joint Surg. Br.40-B(3), 538–545 (1958).
  • Kellgren JH, Lawrence JS, Bier F. Genetic factors in generalized osteo-arthrosis. Ann. Rheum. Dis.22, 237–255 (1963).
  • Nuki G. Osteoarthritis: some genetic approaches. J. Rheumatol. Suppl.9, 29–31 (1983).
  • Lawrence JS, Gelsthorpe K, Morell G. Heberden’s nodes and HLA markers in generalized osteoarthritis. J. Rheumatol. Suppl.9, 32–33 (1983).
  • Hirsch R, Lethbridge-Cejku M, Hanson R et al. Familial aggregation of osteoarthritis: data from the Baltimore Longitudinal Study on Aging. Arthritis Rheum.41(7), 1227–1232 (1998).
  • Felson DT, Couropmitree NN, Chaisson CE et al. Evidence for a Mendelian gene in a segregation analysis of generalized radiographic osteoarthritis: the Framingham Study. Arthritis Rheum.41(6), 1064–1071 (1998).
  • Lindberg H. Prevalence of primary coxarthrosis in siblings of patients with primary coxarthrosis. Clin. Orthop. Relat. Res.203, 273–275 (1986).
  • Chitnavis J, Sinsheimer JS, Clipsham K et al. Genetic influences in end-stage osteoarthritis. Sibling risks of hip and knee replacement for idiopathic osteoarthritis. J. Bone Joint Surg. Br.79(4), 660–664 (1997).
  • Lanyon P, Muir K, Doherty S, Doherty M. Assessment of a genetic contribution to osteoarthritis of the hip: sibling study. Br. Med. J.321(7270), 1179–1183 (2000).
  • Ingvarsson T, Stefansson SE, Hallgrimsdottir IB et al. The inheritance of hip osteoarthritis in Iceland. Arthritis Rheum.43(12), 2785–2792 (2000).
  • Yoo K, Origitano TC. Familial cervical spondylosis. Case report. J. Neurosurg.89(1), 139–141 (1998).
  • Matsui H, Terahata N, Tsuji H, Hirano N, Naruse Y. Familial predisposition and clustering for juvenile lumbar disc herniation. Spine17(11), 1323–1328 (1992).
  • Varlotta GP, Brown MD, Kelsey JL, Golden AL. Familial predisposition for herniation of a lumbar disc in patients who are less than twenty-one years old. J. Bone Joint Surg. Am.73(1), 124–128 (1991).
  • Scapinelli R. Lumbar disc herniation in eight siblings with a positive family history for disc disease. Acta Orthop. Belg.59(4), 371–376 (1993).
  • Spector TD, Cicuttini F, Baker J, Loughlin J, Hart D. Genetic influences on osteoarthritis in women: a twin study. Br. Med. J.312(7036), 940–943 (1996).
  • MacGregor AJ, Antoniades L, Matson M, Andrew T, Spector TD. The genetic contribution to radiographic hip osteoarthritis in women: results of a classic twin study. Arthritis Rheum.43(11), 2410–2416 (2000).
  • Sambrook PN, MacGregor AJ, Spector TD. Genetic influences on cervical and lumbar disc degeneration: a magnetic resonance imaging study in twins. Arthritis Rheum.42(2), 366–372 (1999).
  • Ding C, Cicuttini F, Scott F, Stankovich J, Cooley H, Jones G. The genetic contribution and relevance of knee cartilage defects: case–control and sib-pair studies. J. Rheumatol.32(10), 1937–1942 (2005).
  • Irlenbusch U, Schaller T. Investigations in generalized osteoarthritis. Part 1: genetic study of Heberden’s nodes. Osteoarthr. Cartil.14(5), 423–427 (2006).
  • Kraus VB, Jordan JM, Doherty M et al. The Genetics of Generalized Osteoarthritis (GOGO) study: study design and evaluation of osteoarthritis phenotypes. Osteoarthr. Cartil.15(2), 120–127 (2007).
  • Williams CJ, Jimenez SA. Skeletal dysplasias and the osteoarthritic phenotype. Best Pract. Res. Clin. Rheumatol.17(6), 1005–1018 (2003).
  • Superti-Furga A, Unger S; and the Nosology Group of the Int. Skel. Dyspl. Soc. Nosology and classification of genetic skeletal disorders. Am. J. Med. Genet.143A, 1–18 (2007).
  • Roby P, Eyre S, Worthington J et al. Autosomal dominant (Beukes) premature degenerative osteoarthropathy of the hip joint maps to an 11-cM region on chromosome 4q35. Am. J. Hum. Genet.64(3), 904–908 (1999).
  • Ingvarsson T, Stefansson SE, Gulcher JR et al. A large Icelandic family with early osteoarthritis of the hip associated with a susceptibility locus on chromosome 16p. Arthritis Rheum.44(11), 2548–2555 (2001).
  • Meulenbelt I, Bijkerk C, Breedveld FC, Slagboom PE. Genetic linkage analysis of 14 candidate gene loci in a family with autosomal dominant osteoarthritis without dysplasia. J. Med. Genet.34(12), 1024–1027 (1997).
  • Meulenbelt I, Min JL, van Duijn CM, Kloppenburg M, Breedveld FC, Slagboom PE. Strong linkage on 2q33.3 to familial early-onset generalized osteoarthritis and a consideration of two positional candidate genes. Eur. J. Hum. Genet.14(12), 1280–1287 (2006).
  • Mabuchi A, Nakamura S, Takatori Y, Ikegawa S. Familial osteoarthritis of the hip joint associated with acetabular dysplasia maps to chromosome 13q. Am. J. Hum. Genet.79, 163–168 (2006).
  • Hughes AE, McGibbon D, Woodward E, Dixey J, Doherty M. Localisation of a gene for chondrocalcinosis to chromosome 5p. Hum. Mol. Genet.4(7), 1225–1228 (1995).
  • Andrew LJ, Brancolini V, de la Pena LS et al. Refinement of the chromosome 5p locus for familial calcium pyrophosphate dihydrate deposition disease. Am. J. Hum. Genet.64(1), 136–145 (1999).
  • Pendleton A, Johnson MD, Hughes A et al. Mutations in ANKH cause chondrocalcinosis. Am. J. Hum. Genet.71(4), 933–940 (2002).
  • Williams CJ, Zhang Y, Timms A et al. Autosomal dominant familial calcium pyrophosphate dihydrate deposition disease is caused by mutation in the transmembrane protein ANKH. Am. J. Hum. Genet.71(4), 985–991 (2002).
  • Williams CJ, Pendleton A, Bonavita G et al. Mutations in the amino terminus of ANKH in two US families with calcium pyrophosphate dihydrate crystal deposition disease. Arthritis Rheum.48(9), 2627–2631 (2003).
  • Ho AM, Johnson MD, Kingsley DM. Role of the mouse ank gene in control of tissue calcification and arthritis. Science289(5477), 265–270 (2000).
  • Loughlin J, Irven C, Fergusson C, Sykes B. Sibling pair analysis shows no linkage of generalized osteoarthritis to the loci encoding type II collagen, cartilage link protein or cartilage matrix protein. Br. J. Rheumatol.33(12), 1103–1106 (1994).
  • Mustafa Z, Chapman K, Irven C et al. Linkage analysis of candidate genes as susceptibility loci for osteoarthritis-suggestive linkage of COL9A1 to female hip osteoarthritis. Rheumatology (Oxf.)39(3), 299–306 (2000).
  • Baldwin CT, Cupples LA, Joost O et al. Absence of linkage or association for osteoarthritis with the vitamin D receptor/type II collagen locus: the Framingham Osteoarthritis Study. J. Rheumatol.29(1), 161–165 (2002).
  • Wright GD, Hughes AE, Regan M, Doherty M. Association of two loci on chromosome 2q with nodal osteoarthritis. Ann. Rheum. Dis.55(5), 317–319 (1996).
  • Chapman K, Mustafa Z, Irven C et al. Osteoarthritis-susceptibility locus on chromosome 11q, detected by linkage. Am. J. Hum. Genet.65(1), 167–174 (1999).
  • Leppavuori J, Kujala U, Kinnunen J et al. Genome scan for predisposing loci for distal interphalangeal joint osteoarthritis: evidence for a locus on 2q. Am. J. Hum. Genet.65(4), 1060–1067 (1999).
  • Stankovich J, Sale MM, Cooley HM et al. Investigation of chromosome 2q in osteoarthritis of the hand: no significant linkage in a Tasmanian population. Ann. Rheum. Dis.61(12), 1081–1084 (2002).
  • Loughlin J, Mustafa Z, Irven C et al. Stratification analysis of an osteoarthritis genome screen-suggestive linkage to chromosomes 4, 6, and 16. Am. J. Hum. Genet.65(6), 1795–1798 (1999).
  • Hunter DJ, Demissie S, Cupples LA, Aliabadi P, Felson DT. A genome scan for joint-specific hand osteoarthritis susceptibility: the Framingham Study. Arthritis Rheum.50(8), 2489–2496 (2004).
  • Chapman KL, Mortier GR, Chapman K, Loughlin J, Grant ME, Briggs MD. Mutations in the region encoding the von Willebrand factor A domain of matrilin-3 are associated with multiple epiphyseal dysplasia. Nat. Genet.28(4), 393–396 (2001).
  • Greig C, Spreckley K, Aspinwall R et al. Linkage to nodal osteoarthritis: quantitative and qualitative analyses of data from a whole-genome screen identify trait-dependent susceptibility loci. Ann. Rheum. Dis.65(9), 1131–1138 (2006).
  • Chapman K, Mustafa Z, Dowling B, Southam L, Carr A, Loughlin J. Finer linkage mapping of primary hip osteoarthritis susceptibility on chromosome 11q in a cohort of affected female sibling pairs. Arthritis Rheum.46(7), 1780–1783 (2002).
  • Meenagh GK, McGibbon D, Nixon J, Wright GD, Doherty M, Hughes AE. Lack of support for the presence of an osteoarthritis susceptibility locus on chromosome 6p. Arthritis Rheum.52(7), 2040–2043 (2005).
  • Loughlin J, Mustafa Z, Dowling B et al. Finer linkage mapping of a primary hip osteoarthritis susceptibility locus on chromosome 6. Eur. J. Hum. Genet.10(9), 562–568 (2002).
  • Alizadeh BZ, Njajou OT, Bijkerk C et al. Evidence for a role of the genomic region of the gene encoding for the α1 chain of type IX collagen (COL9A1) in hip osteoarthritis: a population-based study. Arthritis Rheum.52(5), 1437–1442 (2005).
  • Forster T, Chapman K, Marcelline L, Mustafa Z, Southam L, Loughlin J. Finer linkage mapping of primary osteoarthritis susceptibility loci on chromosomes 4 and 16 in families with affected women. Arthritis Rheum.50(1), 98–102 (2004).
  • Tsezou A, Karachalios T, Fytili P et al. Absence of linkage to chromosomes 6q and 16p in a Greek population with knee osteoarthritis. J. Orthop. Res.24(9), 1900–1905 (2006).
  • Riyazi N, Slagboom E, de Craen AJ et al. Association of the risk of osteoarthritis with high innate production of interleukin-1 β and low innate production of interleukin-10 ex vivo, upon lipopolysaccharide stimulation. Arthritis Rheum.52(5), 1443–1450 (2005).
  • Fytili P, Giannatou E, Karachalios T, Malizos K, Tsezou A. Interleukin-10G and interleukin-10R microsatellite polymorphisms and osteoarthritis of the knee. Clin. Exp. Rheumatol.23(5), 621–627 (2005).
  • Mahr S, Burmester GR, Hilke D et al.Cis- and trans-acting gene regulation is associated with osteoarthritis. Am. J. Hum. Genet.78(5), 793–803 (2006).
  • Loughlin J, Meulenbelt I, Min J et al. Genetic association analysis of RHOB and TXNDC3 in osteoarthritis. Am. J. Hum. Genet.80(2), 383–386; author reply 386–387 (2007).
  • Loughlin J, Dowling B, Mustafa Z, Chapman K. Association of the interleukin-1 gene cluster on chromosome 2q13 with knee osteoarthritis. Arthritis Rheum.46(6), 1519–1527 (2002).
  • Stern AG, deCarvalho MR, Buck GA et al. Association of erosive hand osteoarthritis with a single nucleotide polymorphism in the gene encoding interleukin 1 β. Osteoarthr. Cartil..11(6), 394–402 (2003).
  • Meulenbelt I, Seymour AB, Nieuwland M, Huizinga TW, van Duijn CM, Slagboom PE. Association of the interleukin-1 gene cluster with radiographic signs of osteoarthritis of the hip. Arthritis Rheum.50(4), 1179–1186 (2004).
  • Smith AJ, Keen LJ, Billingham MJ et al. Extended haplotypes and linkage disequilibrium in the IL1R1–IL1A–IL1B–IL1RN gene cluster: association with knee osteoarthritis. Genes Immun.5(6), 451–460 (2004).
  • Chapman K, Loughlin J. Association of the interleukin-1 gene cluster with osteoarthritis of the hip: comment on the article by Meulenbelt et al and the letter by Smith et al.Arthritis Rheum.54(11), 3722–3723 (2006).
  • Loughlin J, Dowling B, Chapman K et al. Functional variants within the secreted frizzled-related protein 3 gene are associated with hip osteoarthritis in females. Proc. Natl Acad. Sci. USA101(26), 9757–9762 (2004).
  • Min JL, Meulenbelt I, Riyazi N et al. Association of the Frizzled-related protein gene with symptomatic osteoarthritis at multiple sites. Arthritis Rheum.52(4), 1077–1080 (2005).
  • Lane NE, Lian K, Nevitt MC et al. Frizzled-related protein variants are risk factors for hip osteoarthritis. Arthritis Rheum.54(4), 1246–1254 (2006).
  • Rodriguez-Lopez J, Pombo-Suarez M, Liz M, Gomez-Reino JJ, Gonzalez A. Further evidence of the role of frizzled-related protein gene polymorphisms in osteoarthritis. Ann. Rheum. Dis. DOI: 17237116 (2007) (Epub ahead of print).
  • Ross JM, Kowalchuk RM, Shaulinsky J, Ross L, Ryan D, Phatak PD. Association of heterozygous hemochromatosis C282Y gene mutation with hand osteoarthritis. J. Rheumatol.30(1), 121–125 (2003).
  • Loughlin J, Carr A, Chapman K. The common HFE variants C282Y and H63D are not associated with primary OA of the hip or knee. J. Rheumatol.32(2), 391–392; author reply 392 (2005).
  • Carroll GJ. Primary osteoarthritis in the ankle joint is associated with finger metacarpophalangeal osteoarthritis and the H63D mutation in the HFE gene: evidence for a hemochromatosis-like polyarticular osteoarthritis phenotype. J. Clin. Rheumatol.12(3), 109–113 (2006).
  • Carroll GJ. HFE gene mutations are associated with osteoarthritis in the index or middle finger metacarpophalangeal joints. J. Rheumatol.33(4), 741–743 (2006).
  • Loughlin J, Sinsheimer JS, Mustafa Z et al. Association analysis of the vitamin D receptor gene, the type I collagen gene COL1A1, and the estrogen receptor gene in idiopathic osteoarthritis. J. Rheumatol.27(3), 779–784 (2000).
  • Bergink AP, van Meurs JB, Loughlin J et al. Estrogen receptor α gene haplotype is associated with radiographic osteoarthritis of the knee in elderly men and women. Arthritis Rheum.48(7), 1913–1922 (2003).
  • Jin SY, Hong SJ, Yang HI et al. Estrogen receptor-α gene haplotype is associated with primary knee osteoarthritis in Korean population. Arthritis Res. Ther.6(5), R415–R421 (2004).
  • Fytili P, Giannatou E, Papanikolaou V et al. Association of repeat polymorphisms in the estrogen receptors α, β, and androgen receptor genes with knee osteoarthritis. Clin. Genet.68(3), 268–277 (2005).
  • Kizawa H, Kou I, Iida A et al. An aspartic acid repeat polymorphism in asporin inhibits chondrogenesis and increases susceptibility to osteoarthritis. Nat. Genet.37(2), 138–144 (2005).
  • Mustafa Z, Dowling B, Chapman K, Sinsheimer JS, Carr A, Loughlin J. Investigating the aspartic acid (D) repeat of asporin as a risk factor for osteoarthritis in a UK Caucasian population. Arthritis Rheum.52(11), 3502–3506 (2005).
  • Rodriguez-Lopez J, Pombo-Suarez M, Liz M, Gomez-Reino JJ, Gonzalez A. Lack of association of a variable number of aspartic acid residues in the asporin gene with osteoarthritis susceptibility: case–control studies in Spanish Caucasians. Arthritis Res. Ther.8(3), R55 (2006).
  • Jiang Q, Shi D, Yi L et al. Replication of the association of the aspartic acid repeat polymorphism in the asporin gene with knee-osteoarthritis susceptibility in Han Chinese. J. Hum. Genet.51(12), 1068–1072 (2006).
  • Kaliakatsos M, Tzetis M, Kanavakis E et al. Asporin and knee osteoarthritis in patients of Greek origin. Osteoarthr. Cartil.14, 609–611 (2006).
  • Smith AJ, Gidley J, Sandy JR et al. Haplotypes of the low-density lipoprotein receptor-related protein 5 (LRP5) gene: are they a risk factor in osteoarthritis? Osteoarthr. Cartil.13(7), 608–613 (2005).
  • Urano T, Shiraki M, Narusawa K et al. Q89R polymorphism in the LDL receptor-related protein 5 gene is associated with spinal osteoarthritis in postmenopausal Japanese women. Spine32(1), 25–29 (2007).
  • Priestley L, Fergusson C, Ogilvie D et al. A limited association of generalized osteoarthritis with alleles at the type II collagen locus: COL2A1.Br. J. Rheumatol.30(4), 272–275 (1991).
  • Aerssens J, Dequeker J, Peeters J, Breemans S, Boonen S. Lack of association between osteoarthritis of the hip and gene polymorphisms of VDR, COL1A1, and COL2A1 in postmenopausal women. Arthritis Rheum.41(11), 1946–1950 (1998).
  • Meulenbelt I, Bijkerk C, De Wildt SC et al. Haplotype analysis of three polymorphisms of the COL2A1 gene and associations with generalised radiological osteoarthritis. Ann. Hum. Genet.63(Pt 5), 393–400 (1999).
  • Uitterlinden AG, Burger H, van Duijn CM et al. Adjacent genes, for COL2A1 and the vitamin D receptor, are associated with separate features of radiographic osteoarthritis of the knee. Arthritis Rheum.43(7), 1456–1464 (2000).
  • Uitterlinden AG, Burger H, Huang Q et al. Vitamin D receptor genotype is associated with radiographic osteoarthritis at the knee. J. Clin. Invest.100(2), 259–263 (1997).
  • Keen RW, Hart DJ, Lanchbury JS, Spector TD. Association of early osteoarthritis of the knee with a Taq I polymorphism of the vitamin D receptor gene. Arthritis Rheum.40(8), 1444–1449 (1997).
  • Jordan KM, Syddall H, Dennison EM, Cooper C, Arden NK. Birthweight, vitamin D receptor gene polymorphism, and risk of lumbar spine osteoarthritis. J. Rheumatol.32(4), 678–683 (2005).
  • Solovieva S, Hirvonen A, Siivola P et al. Vitamin D receptor gene polymorphisms and susceptibility of hand osteoarthritis in Finnish women. Arthritis Res. Ther.8(1), R20 (2006).
  • Spector TD, Reneland RH, Mah S et al. Association between a variation in LRCH1 and knee osteoarthritis: a genome-wide single-nucleotide polymorphism association study using DNA pooling. Arthritis Rheum.54(2), 524–532 (2006).
  • Snelling S, Sinsheimer JS, Carr A, Loughlin J. Genetic association analysis of LRCH1 as an osteoarthritis susceptibility locus. Rheumatology46(2), 250–252 (2007).
  • Mototani H, Mabuchi A, Saito S et al. A functional single nucleotide polymorphism in the core promoter region of CALM1 is associated with hip osteoarthritis in Japanese. Hum. Mol. Genet.14(8), 1009–1017 (2005).
  • Loughlin J, Sinsheimer JS, Carr A, Chapman K. The CALM1 core promoter polymorphism is not associated with hip osteoarthritis in a United Kingdom Caucasian population. Osteoarthr. Cartil.14(3), 295–298 (2006).
  • Valdes AM, Loughlin J, Oene MV et al. Sex and ethnic differences in the association of ASPN, CALM1, COL2A1, COMP, and FRZB with genetic susceptibility to osteoarthritis of the knee. Arthritis Rheum.56(1), 137–146 (2007).
  • Lian K, Zmuda JM, Nevitt MC et al. Type I collagen α1 Sp1 transcription factor binding site polymorphism is associated with reduced risk of hip osteoarthritis defined by severe joint space narrowing in elderly women. Arthritis Rheum.52(5), 1431–1436 (2005).
  • Meulenbelt I, Bijkerk C, de Wildt SC et al. Investigation of the association of the CRTM and CRTL1 genes with radiographically evident osteoarthritis in subjects from the Rotterdam study. Arthritis Rheum.40(10), 1760–1765 (1997).
  • Loughlin J, Dowling B, Mustafa Z, Smith A, Sykes B, Chapman K. Analysis of the association of the matrillin-1 gene (CRTM) with osteoarthritis: comment on the article by Meulenbelt et al.Arthritis Rheum.43(6), 1423–1425 (2000).
  • Spector TD, Ahmadi KR, Valdes AM. When is a replication not a replication? Or how to spot a good genetic association study. Arthritis Rheum.54(4), 1051–1054 (2006).
  • Miyamoto Y, Mabuchi A, Shi D et al. A functional polymorphism in the 5´UTR of GDF5 is associated with susceptibility to osteoarthritis. Nat. Genet.39(4), 529–533 (2007).
  • Ikegawa S, Kawamura S, Takahashi A et al. Replication of association of the D-repeat polymorphism in asporin with osteoarthritis (and authors response). Arthritis Res. Ther.8(4), 1–3 (2006).
  • Lee YH, Rho YH, Choi SJ, Ji JD, Song GG. Osteoarthritis susceptibility loci defined by genome scan meta-analysis. Rheumatol. Int.26(11), 959–963 (2006).
  • Aigner T, Fundel K, Saas J et al. Large-scale gene expression profiling reveals major pathogenetic pathways of cartilage degeneration in osteoarthritis. Arthritis Rheum.54(11), 3533–3544 (2006).
  • Valdes AM, Hart DJ, Jones KA et al. Association study of candidate genes for the prevalence and progression of knee osteoarthritis. Arthritis Rheum.50(8), 2497–2507 (2004).
  • Sato T, Konomi K, Yamasaki S et al. Comparative analysis of gene expression profiles in intact and damaged regions of human osteoarthritic cartilage. Arthritis Rheum.54(3), 808–817 (2006).
  • Xiang Y, Sekine T, Nakamura H et al. Fibulin-4 is a target of autoimmunity predominantly in patients with osteoarthritis. J. Immunol.176(5), 3196–3204 (2006).
  • Zhang YW, Su Y, Lanning N et al. Targeted disruption of Mig-6 in the mouse genome leads to early onset degenerative joint disease. Proc. Natl Acad. Sci. USA102(33), 11740–11745 (2005).
  • Min JL, Meulenbelt I, Riyazi N et al. Association of matrilin-3 polymorphisms with spinal disc degeneration and osteoarthritis of the first carpometacarpal joint of the hand. Ann. Rheum. Dis.65(8), 1060–1066 (2006).
  • Pola E, Papaleo P, Pola R et al. Interleukin-6 polymorphism and risk of osteoarthritis of the hip: a case–control study. Osteoarthr. Cartil.13(11), 1025–1028 (2005).
  • Forster T, Chapman K, Loughlin J. Common variants within the interleukin 4 receptor α gene (IL4R) are associated with susceptibility to osteoarthritis. Hum. Genet.114(4), 391–395 (2004).

Website

  • Online Mendelian Inheritance in Man™ www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=OMIM

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.