195
Views
23
CrossRef citations to date
0
Altmetric
Review

Current understanding and management of giant cell arteritis and polymyalgia rheumatica

, &
Pages 913-928 | Published online: 10 Jan 2014

References

  • Machado EB, Michet CJ, Ballard DJ et al. Trends in incidence and clinical presentation of temporal arteritis in Olmsted County, Minnesota, 1950–1985. Arthritis Rheum.31, 745–749 (1988).
  • Salvarani C, Gabriel SE, O’Fallon WM, Hunder GG. Epidemiology of polymyalgia rheumatica in Olmsted County, Minnesota, 1970–1991. Arthritis Rheum.38, 369–373 (1995).
  • Gonzalez-Gay MA, Miranda-Filloy JA, Lopez-Diaz MJ et al. Giant cell arteritis in northwestern Spain: a 25-year epidemiologic study. Medicine (Baltimore)86, 61–68 (2007).
  • González-Gay MA, García-Porrúa C, Vázquez-Caruncho M, Dababneh A, Hajeer A, Ollier WE. The spectrum of polymyalgia rheumatica in northwestern Spain: incidence and analysis of variables associated with relapse in a 10 year study. J. Rheumatol.26, 1326–1332 (1999).
  • Smeeth L, Cook C, Hall AJ. Incidence of diagnosed polymyalgia rheumatica and temporal arteritis in the United Kingdom, 1990–2001. Ann. Rheum. Dis.65, 1093–1098 (2006).
  • Blockmans D, de Ceuninck L, Vanderschueren S, Knockaert D, Mortelmans L, Bobbaers H. Repetitive 18F-fluorodeoxyglucose positron emission tomography in giant cell arteritis: a prospective study of 35 patients. Arthritis Rheum.55, 131–137 (2006).
  • Robbin and Cotran Pathologic Basis of Disease. Kumar VA, Abbas AK, Fausto N (Eds). Elsevier Saunders, PA, USA (2005).
  • Salvarani C, Cantini F, Olivieri I, Hunder GS. Polymyalgia rheumatica: a disorder of extraarticular synovial structures? J. Rheumatol.26, 517–521 (1999).
  • Meliconi R, Pulsatelli L, Uguccioni M et al. Leukocyte infiltration in synovial tissue from the shoulder of patients with polymyalgia rheumatica. Quantitative analysis and influence of corticosteroid treatment. Arthritis Rheum.39, 1199–1207 (1996).
  • Gonzalez-Gay MA, Amoli MM, Garcia-Porrua C, Ollier WE. Genetic markers of disease susceptibility and severity in giant cell arteritis and polymyalgia rheumatica. Semin. Arthritis Rheum.33, 38–48 (2003).
  • Salvarani C, Boiardi L, Mantovani V et al. HLA-DRB1 alleles associated with polymyalgia rheumatica in northern Italy: correlation with disease severity. Ann. Rheum. Dis.58, 303–308 (1999).
  • Hernández-Rodríguez J, García-Martínez A, Casademont J et al. A strong initial systemic inflammatory response is associated with higher corticosteroid requirements and longer duration of therapy in patients with giant-cell arteritis. Arthritis Rheum.47, 29–35 (2002).
  • Mattey DL, Hajeer AH, Dababneh A et al. Association of giant cell arteritis and polymyalgia rheumatica with different tumor necrosis factor microsatellite polymorphisms. Arthritis Rheum.43, 1749–1755 (2000).
  • Gonzalez-Gay MA, Hajeer AH, Dababneh A et al. IL-6 promoter polymorphism at position -174 modulates the phenotypic expression of polymyalgia rheumatica in biopsy-proven giant cell arteritis. Clin. Exp. Rheumatol.20, 179–184 (2002).
  • Makki RF, al Sharif F, González-Gay MA, García-Porrúa C, Ollier WE, Hajeer AH. RANTES gene polymorphism in polymyalgia rheumatica, giant cell arteritis and rheumatoid arthritis. Clin. Exp. Rheumatol.18, 391–393 (2000).
  • Gonzalez-Gay MA, Hajeer AH, Dababneh A et al. Corticotropin releasing hormone promoter polymorphisms in giant cell arteritis and polymyalgia rheumatica. Clin. Exp. Rheumatol.20, 133–138 (2002).
  • Gonzalez-Gay MA, Hajeer AH, Dababneh A et al. Interferon-γ gene microsatellite polymorphisms in patients with biopsy-proven giant cell arteritis and isolated polymyalgia rheumatica. Clin. Exp. Rheumatol.22, S18–S20 (2004).
  • Rueda B, Lopez-Nevot MA, Lopez-Diaz MJ, Garcia-Porrua C, Martín J, Gonzalez-Gay MA. A functional variant of vascular endothelial growth factor is associated with severe ischemic complications in giant cell arteritis. J. Rheumatol.32, 1737–1741 (2005).
  • Segarra M, García-Martínez A, Sánchez M et al. Gelatinase expression and proteolytic activity in giant-cell arteritis. Ann. Rheum. Dis.66, 1429–1435 (2007).
  • Rueda B, Miranda-Filloy JA, Martin J, Gonzalez-Gay MA. Association of CD24 gene polymorphisms with susceptibility to biopsy-proven giant cell arteritis. J. Rheumatol.35, 850–854 (2008).
  • Salvarani C, Gabriel SE, O’Fallon WM, Hunder GG. The incidence of giant cell arteritis in Olmsted County, Minnesota: apparent fluctuations in a cyclic pattern. Ann. Intern. Med.123, 192–194 (1995).
  • Elling P, Olsson AT, Elling H. Synchronous variations of the incidence of temporal arteritis and polymyalgia rheumatica in different regions of Denmark; association with epidemics of Mycoplasma pneumoniae infection. J. Rheumatol.23, 112–119 (1996).
  • Narvaez J, Clavaguera MT, Nolla-Sole JM, Valverde-Garcia J, Roig-Escofet D. Lack of association between infection and onset of polymyalgia rheumatica. J. Rheumatol.27, 953–957 (2000).
  • Wagner AD, Gérard HC, Fresemann T et al. Detection of Chlamydia pneumoniae in giant cell vasculitis and correlation with the topographic arrangement of tissue-infiltrating dendritic cells. Arthritis Rheum.43, 1543–1551 (2000).
  • López-Hoyos M, Alvarez L, Ruiz Soto M, Blanco R, José Bartolomé M, Martínez-Taboada VM. Serum levels of antibodies to Chlamydia pneumoniae and human HSP60 in giant cell arteritis patients. Clin. Exp. Rheumatol.26, 1107–1110 (2008).
  • Brack A, Geisler A, Martinez-Taboada VM, Younge BR, Goronzy JJ, Weyand CM. Giant cell vasculitis is a T cell-dependent disease. Mol. Med.3, 530–543 (1997).
  • Weyand CM, Schönberger J, Oppitz U, Hunder NN, Hicok KC, Goronzy JJ. Distinct vascular lesions in giant cell arteritis share identical T cell clonotypes. J. Exp. Med.179, 951–960 (1994).
  • Ma -Krupa W, Jeon MS, Spoerl S, Tedder TF, Goronzy JJ, Weyand CM. Activation of arterial wall dendritic cells and breakdown of self-tolerance in giant cell arteritis. J. Exp. Med.199, 173–183 (2004).
  • Oriss TB, Ostroukhova M, Seguin-Devaux C et al. Dynamics of dendritic cell phenotype and interactions with CD4+ T cells in airway inflammation and tolerance. J. Immunol.174, 854–863 (2005).
  • Lau AH, Thomson AW. Dendritic cells and immune regulation in the liver. Gut52, 307–314 (2003).
  • Pryshchep O, Ma-Krupa W, Younge BR, Goronzy JJ, Weyand CM. Vessel-specific Toll-like receptor profiles in human medium and large arteries. Circulation118, 1276–1284 (2008).
  • Otero C, Eisele PS, Schaeuble K, Groettrup M, Legler DF. Distinct motifs in the chemokine receptor CCR7 regulate signal transduction, receptor trafficking and chemotaxis. J. Cell. Sci.121, 2759–2767 (2008).
  • Krupa WM, Dewan M, Jeon MS et al. Trapping of misdirected dendritic cells in the granulomatous lesions of giant cell arteritis. Am. J. Pathol.161, 1815–1823 (2002).
  • Cid MC, Hoffman MP, Hernández-Rodríguez J et al. Association between increased CCL2 (MCP-1) expression in lesions and persistence of disease activity in giant-cell arteritis. Rheumatology (Oxford)45, 1356–1363 (2006).
  • Martinez-Taboada VM, Alvarez L, RuizSoto M, Marin-Vidalled MJ, Lopez-Hoyos M. Giant cell arteritis and polymyalgia rheumatica: role of cytokines in the pathogenesis and implications for treatment. Cytokine44, 207–220 (2008).
  • Cutolo M, Straub RH, Foppiani L et al. Adrenal gland hypofunction in active polymyalgia rheumatica. effect of glucocorticoid treatment on adrenal hormones and interleukin 6. J. Rheumatol.29, 748–756 (2002).
  • Ross R. Cellular and molecular studies of atherogenesis. Atherosclerosis131(Suppl.), S3–S4 (1997).
  • Salvarani C, Macchioni PL, Tartoni PL et al. Polymyalgia rheumatica and giant cell arteritis: a 5-year epidemiologic and clinical study in Reggio Emilia, Italy. Clin. Exp. Rheumatol.5, 205–215 (1987).
  • Makkuni D, Bharadwaj A, Wolfe K, Payne S, Hutchings A, Dasgupta B. Is intimal hyperplasia a marker of neuro-ophthalmic complications of giant cell arteritis? Rheumatology (Oxford)47, 488–490 (2008).
  • Pulsatelli L, Dolzani P, Silvestri T et al. Synovial expression of vasoactive intestinal peptide in polymyalgia rheumatica. Clin. Exp. Rheumatol.24, 562–566 (2006).
  • Emilie D, Liozon E, Crevon MC et al. Production of interleukin 6 by granulomas of giant cell arteritis. Hum. Immunol.39, 17–24 (1994).
  • Lecron JC, Roblot P, Chevalier S et al. High circulating leukaemia inhibitory factor (LIF) in patients with giant cell arteritis: independent regulation of LIF and IL-6 under corticosteroid therapy. Clin. Exp. Immunol.92, 23–26 (1993).
  • Roche NE, Fulbright JW, Wagner AD, Hunder GG, Goronzy JJ, Weyand CM. Correlation of interleukin-6 production and disease activity in polymyalgia rheumatica and giant cell arteritis. Arthritis Rheum.36, 1286–1294 (1993).
  • Uddhammar A, Sundqvist KG, Ellis B, Rantapaa-Dahlqvist S. Cytokines and adhesion molecules in patients with polymyalgia rheumatica. Br. J. Rheumatol.37, 766–769 (1998).
  • Roblot P, Morel F, Lelievre E, Gascan H, Wijdenes J, Lecron JC. Serum cytokine and cytokine receptor levels in patients with giant cell arteritis during corticotherapy. J. Rheumatol.23, 408–410 (1996).
  • Straub RH, Herfarth HH, Rinkes B et al. Favorable role of interleukin 10 in patients with polymyalgia rheumatica. J. Rheumatol.26, 1318–1325 (1999).
  • Cutolo M, Montecucco CM, Cavagna L et al. Serum cytokines and steroidal hormones in polymyalgia rheumatica and elderly-onset rheumatoid arthritis. Ann. Rheum. Dis.65, 1438–1443 (2006).
  • Corrigall VM, Dolan AL, Dasgupta B, Panayi GS. The sequential analysis of T lymphocyte subsets and interleukin-6 in polymyalgia rheumatica patients as predictors of disease remission and steroid withdrawal. Br. J. Rheumatol.36, 976–980 (1997).
  • Hernandez-Rodriguez J, Segarra M, Vilardell C et al. Tissue production of pro-inflammatory cytokines (IL-1β, TNF-α and IL-6) correlates with the intensity of the systemic inflammatory response and with corticosteroid requirements in giant-cell arteritis. Rheumatology (Oxford)43, 294–301 (2004).
  • Hernandez-Rodriguez J, Segarra M, Vilardell C et al. Elevated production of interleukin-6 is associated with a lower incidence of disease-related ischemic events in patients with giant-cell arteritis: angiogenic activity of interleukin-6 as a potential protective mechanism. Circulation107, 2428–2434 (2003).
  • Weyand CM, Fulbright JW, Hunder GG, Evans JM, Goronzy JJ. Treatment of giant cell arteritis: interleukin-6 as a biologic marker of disease activity. Arthritis Rheum.43, 1041–1048 (2000).
  • Weyand CM, Wagner AD, Bjornsson J, Goronzy JJ. Correlation of the topographical arrangement and the functional pattern of tissue-infiltrating macrophages in giant cell arteritis. J. Clin. Invest.98, 1642–1649 (1996).
  • Hunder GG, Bloch DA, Michel BA et al. The American College of Rheumatology 1990 criteria for the classification of giant cell arteritis. Arthritis Rheum.33, 1122–1128 (1990).
  • Brooks RC, McGee SR. Diagnostic dilemmas in polymyalgia rheumatica. Arch. Intern. Med.157, 162–168 (1997).
  • Gonzalez-Gay MA, Garcia-Porrua C, Salvarani C, Olivieri I, Hunder GG. The spectrum of conditions mimicking polymyalgia rheumatica in Northwestern Spain. J. Rheumatol.27, 2179–2184 (2000).
  • Gonzalez-Gay MA, Garcia-Porrua C, Salvarani C, Olivieri I, Hunder GG. Polymyalgia manifestations in different conditions mimicking polymyalgia rheumatica. Clin. Exp. Rheumatol.18, 755–759 (2000).
  • Bird HA, Esselinckx W, Dixon AS, Mowat AG, Wood PH. An evaluation of criteria for polymyalgia rheumatica. Ann. Rheum. Dis.38, 434–439 (1979).
  • Chuang TY, Hunder GG, Ilstrup DM, Kurland LT. Polymyalgia rheumatica: a 10-year epidemiologic and clinical study. Ann. Intern. Med.97, 672–680 (1982).
  • Jones JG, Hazleman BL. Prognosis and management of polymyalgia rheumatica. Ann. Rheum. Dis.40, 1–5 (1981).
  • Healey LA. Long-term follow-up of polymyalgia rheumatica: evidence for synovitis. Semin. Arthritis Rheum.13, 322–328 (1984).
  • Dasgupta B, Salvarani C, Schirmer M et al. Developing classification criteria for polymyalgia rheumatica: comparison of views from an expert panel and wider survey. J. Rheumatol.35, 270–277 (2008).
  • Gonzalez-Gay MA, Barros S, Lopez-Diaz MJ, Garcia-Porrua C, Sanchez-Andrade A, Llorca J. Giant cell arteritis: disease patterns of clinical presentation in a series of 240 patients. Medicine (Baltimore)84, 269–276 (2005).
  • Gonzalez-Gay MA, Garcia-Porrua C, Amor-Dorado JC, Llorca J. Fever in biopsy-proven giant cell arteritis: clinical implications in a defined population. Arthritis Rheum.51, 652–655 (2004).
  • Gonzalez-Gay MA, Garcia-Porrua C, Amor-Dorado JC, Llorca, J. Giant cell arteritis without clinically evident vascular involvement in a defined population. Arthritis Rheum.51, 274–277 (2004).
  • González-Gay MA, García-Porrúa C, Llorca J et al. Visual manifestations of giant cell arteritis. Trends and clinical spectrum in 161 patients. Medicine (Baltimore)79, 283–292 (2000).
  • Nuenninghoff DM, Hunder GG, Christianson TJ, McClelland RL, Matteson EL. Incidence and predictors of large-artery complication (aortic aneurysm, aortic dissection, and/or large-artery stenosis) in patients with giant cell arteritis: a population-based study over 50 years. Arthritis Rheum.48, 3522–3531 (2003).
  • Penn H, Dasgupta B. Giant cell arteritis. Autoimmun. Rev.2, 199–203 (2003).
  • Franzen P, Sutinen S, von Knorring J. Giant cell arteritis and polymyalgia rheumatica in a region of Finland: an epidemiologic, clinical and pathologic study, 1984–1988. J. Rheumatol.19, 273–276 (1992).
  • Smetana GW, Shmerling RH. Does this patient have temporal arteritis? JAMA287, 92–101 (2002).
  • Schmidt WA, Kraft HE, Vorpahl K, Volker L, Gromnica-Ihle EJ. Color duplex ultrasonography in the diagnosis of temporal arteritis. N. Engl. J. Med.337, 1336–1342 (1997).
  • Karassa FB, Matsagas MI, Schmidt WA, Ioannidis JP. Meta-analysis: test performance of ultrasonography for giant-cell arteritis. Ann. Intern. Med.142, 359–369 (2005).
  • Blockmans D, Coudyzer W, Vanderschueren S et al. Relationship between fluorodeoxyglucose uptake in the large vessels and late aortic diameter in giant cell arteritis. Rheumatology (Oxford)47, 1179–1184 (2008).
  • Bley TA, Uhl M, Carew J et al. Diagnostic value of high-resolution MR imaging in giant cell arteritis. AJNR Am. J. Neuroradiol.28, 1722–1727 (2007).
  • Dasgupta B, Hutchings A, Matteson EL. Polymyalgia rheumatica: the mess we are now in and what we need to do about it. Arthritis Rheum.55, 518–520 (2006).
  • Bahlas S, Ramos-Remus C, Davis P. Utilisation and costs of investigations, and accuracy of diagnosis of polymyalgia rheumatica by family physicians. Clin. Rheumatol.19, 278–280 (2000).
  • Frediani B, Falsetti P, Storri L et al. Evidence for synovitis in active polymyalgia rheumatica: sonographic study in a large series of patients. J. Rheumatol.29, 123–130 (2002).
  • McGonagle D, Pease C, Marzo-Ortega H et al. Comparison of extracapsular changes by magnetic resonance imaging in patients with rheumatoid arthritis and polymyalgia rheumatica. J. Rheumatol.28, 1837–1841 (2001).
  • Cantini F, Niccoli L, Nannini C et al. Inflammatory changes of hip synovial structures in polymyalgia rheumatica. Clin. Exp. Rheumatol.23, 462–468 (2005).
  • Salvarani C, Cantini F, Olivieri I et al. Proximal bursitis in active polymyalgia rheumatica. Ann. Int. Med.127, 27–31 (1997).
  • Lange U, Piegsa M, Teichmann J, Neeck G. Ultrasonography of the glenohumeral joints – a helpful instrument in differentiation in elderly onset rheumatoid arthritis and polymyalgia rheumatica. Rheumatol. Int.19, 185–189 (2000).
  • Cantini F, Salvarani C, Olivieri I et al. Inflamed shoulder structures in polymyalgia rheumatica with normal erythrocyte sedimentation rate. Arthritis Rheum.44, 1155–1159 (2001).
  • Salvarani C, Barozzi L, Cantini F et al. Cervical interspinous bursitis in active polymyalgia rheumatica. Ann. Rheum. Dis.67, 758–761 (2008).
  • Dasgupta B, Borg FA, Hassan N et al. BSR and BHPR guidelines for the management of giant cell arteritis. Rheumatology (Oxford)49, 1594–1597 (2010).
  • Dasgupta B, Borg FA, Hassan N et al. BSR and BHPR guidelines for the management of polymyalgia rheumatica. Rheumatology (Oxford)49, 186–190 (2010).
  • Loddenkemper T, Sharma P, Katzan I, Plant GT. Risk factors for early visual deterioration in temporal arteritis. J. Neurol. Neurosurg. Psychiatry78, 1255–1259 (2007).
  • Tarkkanen A. Giant cell arteritis and the ophthalmologist. Acta Ophthalmol. Scand.80, 353–354 (2002).
  • Hayreh SS, Zimmerman B. Visual deterioration in giant cell arteritis patients while on high doses of corticosteroid therapy. Ophthalmology110, 1204–1215 (2003).
  • Proven A, Gabriel SE, Orces C, O’Fallon WM, Hunder GG. Glucocorticoid therapy in giant cell arteritis: duration and adverse outcomes. Arthritis Rheum.49, 703–708 (2003).
  • Mazlumzadeh M, Hunder GG, Easley KA et al. Treatment of giant cell arteritis using induction therapy with high-dose glucocorticoids: a double-blind, placebo-controlled, randomized prospective clinical trial. Arthritis Rheum.54, 3310–3318 (2006).
  • Weyand CM, Kaiser M, Yang H, Younge B, Goronzy JJ. Therapeutic effects of acetylsalicylic acid in giant cell arteritis. Arthritis Rheum.46, 457–466 (2002).
  • Nesher G, Berkun Y, Mates M, Baras M, Rubinow A, Sonnenblick M. Low-dose aspirin and prevention of cranial ischemic complications in giant cell arteritis. Arthritis Rheum.50, 1332–1337 (2004).
  • Narváez J, Bernad B, Gómez-Vaquero C et al. Impact of antiplatelet therapy in the development of severe ischemic complications and in the outcome of patients with giant cell arteritis. Clin. Exp. Rheumatol.26, S57–S62 (2008).
  • Gonzalez-Gay MA, Piñeiro A, Gomez-Gigirey A et al. Influence of traditional risk factors of atherosclerosis in the development of severe ischemic complications in giant cell arteritis. Medicine (Baltimore)83, 342–347 (2004).
  • Berger CT, Wolbers M, Meyer P, Daikeler T, Hess C. High incidence of severe ischaemic complications in patients with giant cell arteritis irrespective of platelet count and size, and platelet inhibition. Rheumatology (Oxford)48, 258–261 (2009).
  • Salvarani C, Della Bella C, Cimino L et al. Risk factors for severe cranial ischaemic events in an Italian population-based cohort of patients with giant cell arteritis. Rheumatology (Oxford)48, 250–253 (2009).
  • Hoffman GS, Cid MC, Rendt-Zagar KE et al. Infliximab for maintenance of glucocorticosteroid-induced remission of giant cell arteritis: a randomized trial. Ann. Intern. Med.146, 621–630 (2007).
  • Mahr AD, Jova JA, Spiera RF et al. Adjunctive methotrexate for treatment of giant cell arteritis: an individual patient data meta-analysis. Arthritis Rheum.56, 2789–2797 (2007).
  • De Silva M, Hazleman BL. Azathioprine in giant cell arteritis/polymyalgia rheumatica: a double-blind study. Ann. Rheum. Dis.45, 136–138 (1986).
  • Dharmapaliah C, Borg F, Dasgupta B. Efficacy and tolerability of leflunomide in difficult-to-treat polymyalgia rheumatica and giant cell arteritis: a case series. Rheumatology (Oxford)48, i42 (2009).
  • Cantini F, Niccoli L, Salvarani C, Padula A, Olivieri I. Treatment of longstanding active giant cell arteritis with infliximab: report of four cases. Arthritis Rheum.44, 2933–2935 (2001).
  • Bhatia A, Ell PJ, Edwards JC. Anti-CD20 monoclonal antibody (rituximab) as an adjunct in the treatment of giant cell arteritis. Ann. Rheum. Dis.64, 1099–1100 (2005).
  • Mayrbaeurl B, Hinterreiter M, Burgstaller S, Windpessl M, Thaler J. The first case of a patient with neutropenia and giant-cell arteritis treated with rituximab. Clin. Rheumatol.26, 1597–1598 (2007).
  • Martínez-Taboada VM, Rodríguez-Valverde V, Carreño L et al. A double-blind placebo controlled trial of etanercept in patients with giant cell arteritis and corticosteroid side effects. Ann. Rheum. Dis.67, 625–630 (2008).
  • Catoggio W, Soriano ER, Imamura PM. Treatment of polymyalgia rheumatica: lower initial dose. Br. J. Rheumatol.30, 393–395 (1991).
  • Kremers HM, Reinalda MS, Crowson CS et al. Relapse in a population based cohort of patients with polymyalgia rheumatica. J. Rheumatol.32, 65–73 (2005).
  • Caporali R, Cimmino MA, Ferraccioli G et al. Prednisone plus methotrexate for polymyalgia rheumatica: a randomized, double-blind, placebo-controlled trial. Ann. Intern. Med.141, 493–500 (2004).
  • Salvarani C, Macchioni P, Manzini C et al. Infliximab plus prednisone or placebo plus prednisone for the initial treatment of polymyalgia rheumatica: a randomized trial. Ann. Intern. Med.146, 631–639 (2007).
  • Catanoso MG, Macchioni P, Boiardi L, Pipitone N, Salvarani C. Treatment of refractory polymyalgia rheumatica with etanercept: an open pilot study. Arthritis Rheum.57, 1514–1519 (2007).
  • Warrington KJ, Jarpa EP, Crowson CS et al. Increased risk of peripheral arterial disease in polymyalgia rheumatica: a population-based cohort study. Arthritis Res. Ther.11, R50 (2009).

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.