Advanced search
Publication Cover
Expert Review of Clinical Immunology Volume 4, 2008 - Issue 3
Submit an article Journal homepage
99
Views
29
CrossRef citations to date
0
Altmetric
Review

Rationale and efficacy for the use of rituximab in paraneoplastic pemphigus

Pamela Vezzoli Institute of Dermatological Sciences, University of Milan - Fondazione IRCCS Ospedale Maggiore Policlinico Mangiagalli e Regina Elena, via Pace 9, 20122 Milan, Italy. [email protected]
,
Emilio Berti University of Milan - Bicocca Department of Dermatology (DIMEP), via Cadore 48, Monza, Italy
&
Angelo V Marzano Institute of Dermatological Sciences, University of Milan - Fondazione IRCCS Ospedale Maggiore Policlinico Mangiagalli e Regina Elena, via Pace 9, 20122 Milan, Italy
Pages 351-363 | Published online: 10 Jan 2014

References

  • Anhalt GJ, Kim SC, Stanley JR et al. Paraneoplastic pemphigus, an autoimmune disease associated with neoplasia. N. Engl. J. Med.323, 1729–1735 (1990).
  • Liu AY, Valenzuela R, Helm TN, Camisa C, Melton AL, Bergfeld WF. Indirect immunofluorescence on rat bladder transitional epithelium: a test with high specificity for paraneoplastic pemphigus. J. Am. Acad. Dermatol.28, 696–699 (1993).
  • Anhalt GJ. Paraneoplastic pemphigus. J. Invest. Dermatol. Symp. Proc.9, 29–33 (2004).
  • Joly P, Richard C, Gilbert D et al. Sensitivity and specificity of clinical, histologic and immunologic features in the diagnosis of paraneoplastic pemphigus. J. Am. Acad. Dermatol.43, 619–626 (2000).
  • Nguyen VT, Ndoye A, Bassler KD et al. Classification, clinical manifestations, and immunopathological mechanisms of the epithelial variant of paraneoplastic autoimmune multiorgan syndrome. Arch. Dermatol.137, 193–207 (2001).
  • Robinson ND, Hashimoto T, Amagai M, Chan LS. The new pemphigus variants. J. Am. Acad. Dermatol.40, 649–671 (1999).
  • Schlesinger T, McCarron K, Camisa C, Anhalt G. Paraneoplastic pemphigus occurring in a patient with B-cell non-Hodgkin’s lymphoma. Cutis61, 94–96 (1998).
  • Plumb R, Doolittle GC. Paraneoplastic pemphigus in a patient with non-Hodgkin’s lymphoma. Am. J. Hematol.52, 58–59 (1996).
  • Marzano AV, Grammatica A, Cozzani E, Terracina M, Berti E. Paraneoplastic pemphigus. A report of two cases associated with chronic B-cell lymphocytic leukaemia. Br. J. Dermatol.145, 127–131(2001).
  • Jansen T, Plewig G, Anhalt GJ. Paraneoplastic pemphigus with clinical features of erosive lichen planus associated with Castleman’s tumor. Dermatology190, 245–250 (1995).
  • Lemon MA, Weston WL, Huff JC. Childhood paraneoplastic pemphigus associated with Castleman’s tumour. Br. J. Dermatol.136, 115–117 (1997).
  • Kim SC, Chang SN, Lee IJ et al. Localized mucosal involvement in a young patient with paraneoplastic pemphigus associated with Castleman’s tumour. Br. J. Dermatol.138, 667–671 (1998).
  • Wolff H, Kunte C, Messer G et al. Paraneoplastic pemphigus with fatal pulmonary involvement in a woman with a mesenteric Castleman tumour. Br. J. Dermatol.140, 313–316 (1999).
  • Lee IJ, Kim SC, Kim HS et al. Paraneoplastic pemphigus associated with follicular dendritic cell sarcoma arising from Castleman’s tumor. J. Am. Acad. Dermatol.40, 294–297 (1999).
  • Irsutti M, Paul JL, Selves J, Railhac JJ. Castleman disease: CT and MR imaging features of a retroperitoneal location in association with paraneoplastic pemphigus. Eur. Radiol.9, 1219–1221 (1999).
  • Chorzelski T, Hashimoto T, Maciejewska B, Amagai M, Anhalt GJ, Jablonska S. Paraneoplastic pemphigus associated with Castleman’s tumor, myasthenia gravis and bronchiolitis obliterans. J. Am. Acad. Dermatol.41, 393–400 (1999).
  • Hsiao CJ, Hsu MML, Lee JYY, Chen WC, Hsieh WC. Paraneoplastic pemphigus in association with a retroperitoneal Castleman’s disease presenting with a lichen planus pemphigoides-like eruption. A case and review of literature. Br. J. Dermatol.144, 372–376 (2001).
  • Chin AC, Stich D, White FV, Radhacrishnan J, Holterman MJ. Paraneoplastic pemphigus and bronchiolitis obliterans associated with a mediastinal mass: a rare case of Castleman’s disease with respiratory failure requiring lung transplantation. J. Pediatr. Surg.36, E22 (2001).
  • Fujimoto W, Kanehiro A, Kuwamoto-Hara K et al. Paraneoplastic pemphigus associated with Castleman’s disease and asymptomatic bronchiolitis obliterans. Eur. J. Dermatol.12, 355–359 (2002).
  • Wang L, Bu D, Yang Y, Chen X, Zhu H. Castleman’s tumours and production of autoantibody in paraneoplastic pemphigus. Lancet363, 525–531 (2004).
  • Hinterhuber G, Drach J, Riedl E et al. Paraneoplastic pemphigus in association with hepatocellular carcinoma. J. Am. Acad. Dermatol.49, 538–540 (2003).
  • Niimi Y, Kawana S, Hashimoto T, Kusunoki T. Paraneoplastic pemphigus associated with uterine carcinoma. J. Am. Acad. Dermatol.48, S69–S72 (2003).
  • Kaplan I, Hodak E, Ackerman L, Mimouni D, Anhalt GJ, Calderon S. Neoplasms associated with paraneoplastic pemphigus: a review with emphasis or non-hematologic malignancy and oral mucosal manifestations. Oral. Oncol.40(6), 553–562 (2004).
  • Anhalt GJ. Paraneoplastic pemphigus. Adv. Dermatol.12, 77–96 (1997).
  • Younus J, Ahmed AR. The relationship of pemphigus to neoplasia. J. Am. Acad. Dermatol.23, 498–502 (1990).
  • De Saint PG, Albes B, Bayle P, Lamant L, Bazex J. Cutaneous T-cell lymphoma, cutaneous hyperpigmentation and paraneoplastic pemphigus. Ann. Dermatol. Venereol.129, 896–900 (2002).
  • Marzano AV, Vezzoli P, Mariotti F, Boneschi V, Caputo R, Berti E. Paraneoplastic pemphigus associated with follicular dendritic cell sarcoma and Castleman disease. Br. J. Dermatol.153(1), 214–215 (2005).
  • Park GT, Lee JH, Yun SJ, Lee SC, Lee JB. Paraneoplastic pemphigus without an underlying neoplasm. Br. J. Dermatol.156, 563–566 (2007).
  • Ostezan LB, Fabre VC, Caughman SW, Swerlick RA, Korman NJ, Callen JP. Paraneoplastic pemphigus in the absence of a known neoplasm. J. Am. Acad. Dermatol.33, 312–315 (1995).
  • Mimouni D, Anhalt GJ, Lazarova Z et al. Paraneoplastic pemphigus in children and adolescents. Br. J. Dermatol.147, 725–732 (2002).
  • Lane JE, Woody C, Davis LS, Guill MF, Jerath RS. Paraneoplastic autoimmune multiorgan syndrome (paraneoplastic pemphigus) in a child: case report and review of the literature. Pediatrics114, 513–516 (2004).
  • Wang J, Bu DF, Li T et al. Autoantibody production from a thymoma and a follicular dendritic cell sarcoma associated with paraneoplastic pemphigus. Br. J. Dermatol.153, 558–564 (2005).
  • Bowen GM, Peters NT, Fivenson DP et al. Lichenoid dermatitis in paraneoplastic pemphigus: a pathogenetic trigger of epitope spreading? Arch. Dermatol.136, 652–656 (2000).
  • Chan LS. Epitope spreading in paraneoplastic pemphigus: autoimmune induction in antibody-mediated blistering skin diseases. Arch. Dermatol.136, 663–664 (2000).
  • Zhu X, Zhang B. Paraneoplastic pemphigus. J. Dermatol.34, 503–511 (2007).
  • Zhang B, Zheng R, Wang J, Bu D, Zhu X. Epitopes in the linker subdomain region of envoplakin recognized by autoantibodies in paraneoplastic pemphigus patients. J. Invest. Dermatol.126, 832–840 (2006).
  • Taams LS, Smith J, Rustin MH, Salmon M, Poulter LW, Akbar AN. Human anergic/suppressive CD4(+)CD25(+) T cells: a highly differentiated and apoptosis-prone population. Eur. J. Immunol.31, 1122–1131 (2001).
  • Reich K, Brinck U, Letschert M et al. Graft-versus-host-disease-like immunophenotype and apoptotic keratinocyte in paraneoplastic pemphigus. Br. J. Dermatol.141, 739–746 (1999).
  • Powell AM, Albert S, Oyama N, Sakuma-Oyama Y, Bhogal B, Black MM. Paraneoplastic pemphigus secondary to fludarabine evolving into unusual oral pemphigus vegetans. JEADV18, 360–364 (2004).
  • Gooptu C, Littlewood TJ, Frith P, Lyon CC, Carmichael AJ, Oliwiecki S. Paraneoplastic pemphigus: an association with fludarabine? Br. J. Dermatol.144(66), 1255–1261 (2001).
  • Menenakos C, Braumann C, Hartmann C, Jacobi CA. Retroperitoneal Castleman’s tumor and paraneoplastic pemphigus: report of a case and review of the literature. World J. Surg. Oncol.5, 45 (2007).
  • Nousari HC, Deterding R, Wojtczack H et al. The mechanism of respiratory failure in paraneoplastic pemphigus. N. Engl. J. Med.340, 1406–1410 (1999).
  • Nikolskaia OV, Nousari CH, Anhalt GJ. Paraneoplastic pemphigus in association with Castleman’s disease. Br. J. Dermatol.149, 1143–1151 (2003).
  • Cummins DL, Mimouni D, Tzu J, Owens N, Anhalt GJ, Meyerle JH. Lichenoid paraneoplastic pemphigus in the absence of detectable antibodies J. Am. Acad. Dermatol.56, 153–159 (2007).
  • Hoffman MA, Qiao X, Anhalt GJ. CD8+ T lymphocytes in bronchiolitis obliterans, paraneoplastic pemphigus, and solitary Castleman’s disease. N. Engl. J. Med.24(349), 407–408 (2003).
  • Sun H, Wang R, Bin H et al. Localized Castleman’s disease with paraneoplastic pemphigus and pulmonary involvement, clinical features and histopathology. Zhonghua Yi Xue Za Zhi82, 530–533 (2002).
  • Heymann WR. Paraneoplastic autoimmune multiorgan syndrome. J. Am. Acad. Dermatol.51, 631–632 (2004).
  • Wang J, Zhu X, Li R et al. Paraneoplastic pemphigus associated with Castleman tumor: a commonly reported subtype of paraneoplastic pemphigus in China. Arch. Dermatol.141, 1285–1293 (2005).
  • Quartier P, Brethon B, Philippet P, Landman-Parker J, Le Deist F, Fisher A. Treatment of childhood autoimmune haemolytic anaemia with rituximab. Lancet358, 1511–1513 (2001).
  • Specks U, Fervenza FC, McDonald TJ, Hogan MC. Response of Wegener’s granulomatosis to anti-CD20 chimeric monoclonal antibody therapy. Arthritis Rheum.44, 2836–2840 (2001).
  • Stasi R, Pagano A, Stipa E, Amadori S. Rituximab chimeric anti-CD20 monoclonal antibody treatment for adults with chronic idiopathic thrombocytopenic purpura. Blood98, 952–957 (2001).
  • Grillo-Lopez AJ, White CA, Dallaire BK et al. Rituximab: the first monoclonal antibody approved for the treatment of lymphoma. Curr. Pharm. Biotechnol.1, 1–9 (2000).
  • Virgolini L, Marzocchi V. Rituximab in autoimmune diseases. Biomed. Pharmacother.58, 299–309 (2004).
  • Byrd JC, Waselenko JK, Maneatis TJ et al. Rituximab therapy in hematologic malignancy patients with circulating blood tumor cells: association with increased infusion-related side effects and rapid blood tumor clearance. J. Clin. Oncol.17, 791–795 (1999).
  • Lowndes S, Darby A, Mead G et al. Stevens–Johnson syndrome after treatment with rituximab. Ann. Oncol.13, 1948–1950 (2002).
  • Borradori L, Lombardi T, Samson J et al. Anti-CD20 monoclonal antibody (rituxiamb) for refractory erosive stomatits secondary to CD20+ follicular lymphoma-associated paraneoplastic pemphigus. Arch. Dermatol.137, 269–272 (2001).
  • Heizmann M, Itin P, Wernli M, Borradori L, Bargentzi MJ. Successful treatment of paraneoplastic pemphigus in follicular NHL with rituximab: report of a case and review of treatment for paraneoplastic pemphigus in NHL and CLL. Am. J. Hematol.66, 142–144 (2001).
  • Barnadas MA, Roe E, Brunet S et al. Therapy of paraneoplastic pemphigus with rituximab: a case report and review of literature. JEADV20, 69–74 (2006).
  • Vecchietti G, Kerl K, Hügli A, Samson J, Borradori L. Topical tacrolimus (FK506) for relapsing erosive stomatitis in paraneoplastic pemphigus. Br. J. Dermatol.148, 823–842 (2003).
  • Ahmed Razzaque A, Avram MM, Duncan LM. Case 23–2003: a 79-year-old woman with gastric lymphoma and erosive mucosal and cutaneous lesions. N. Engl. J. Med.349, 382–391 (2003).
  • Van Rossum MM, Verhaegen NT, Jonkman MF et al. Follicular non-Hodgkin’s lymphoma with refractory paraneoplastic pemphigus: case report with review of novel treatment modalities. Leukemia Lymphoma45(11), 2327–2332 (2004).
  • Schadlow MB, Anhalt GJ, Sinha AA. Using rituximab (anti-CD20 antibody) in a patient with paraneoplastic pemphigus. J. Drugs Dermatol.2, 564–567 (2003).
  • Hoque SR, Black MM, Cliff S. Paraneoplastic pemphigus associated with CD20-positive follicular non-Hodgkin’s lymphoma treated with rituximab: a third case resistant to rituximab therapy. Clin. Exp. Dermatol.32, 172–175 (2007).
  • Zaja F, Russo D, Fuga G, Perella G, Baccarani M. Rituximab for myasthenia gravis developing after bone marrow transplant. Neurology55, 1062–1063 (2000).
  • Ratanatharathorn V, Carson E, Reynolds C, Ayash LJ, Levine J, Yanik G. Anti-CD20 chimeric monoclonal antibody treatment of refractory immune-mediated thrombocytopenia in a patient with chronic graft-versus-host disease. Ann. Intern. Med.133, 275–279 (2000).
  • Shvidel L, Klepfish A, Berrebi A. Succesful treatment with rituximab for relapsing immune thrombocytopenic purpura (ITP) associated with low-grade non-Hodgkin’s lymphoma. Am. J. Hematol.67, 213–219 (2001).
  • Marzano AV, Fanoni D, Venegoni L, Berti E, Caputo R. Treatment of refractory pemphigus with the anti-CD20 monoclonal antibody (rituximab). Dermatology214, 310–318 (2007).
  • Salopeck TG, Logsetty S, Tredger EE. Anti-CD20 chimeric monoclonal antibody (rituximab) for the treatment of recalcitrant, life-threatening pemphigus vulgaris with implications in the pathogenesis of the disorder. J. Am. Acad. Dermatol.47, 785–788 (2002).
  • España E, Fernández-Galar M, Lloret P, Sánchez-Ibarrola A, Panizo C. Long-term complete remission of severe pemphigus vulgaris with monoclonal anti-CD20 antibody therapy and immunophenotype correlations. J. Am. Acad. Dermatol.50, 974–976 (2004).
  • Arin MJ, Hunzelmann N. Anti-B-cell-directed immunotherapy (rituximab) in the treatment of refractory pemphigus –an update. Eur. J. Dermatol.15, 224–230 (2005).
  • Niedermeier A, Worl P, Barth S, Schuler G, Hertl M. Delayed response of oral pemphigus vulgaris to rituximab treatment. Eur. J. Dermatol.16, 266–270 (2006).
  • Niedermeier A, Eming R, Pfutze M et al. Clinical response of severe mechanobullous epidermolysis bullosa acquisita to combined treatment with immunoadsorption and rituximab (anti-CD20 monoclonal antibody). Arch. Dermatol.143, 192–198 (2007).
  • Schmidh E, Seitz CS, Benoit S, Brocker EB, Goebeler M. Rituximab in autoimmune bullous diseases: mixed responses and adverse effects. Br. J. Dermatol.156, 352–356 (2007).
  • Ahmed AR, Spigelman Z, Cavacini LA, Posner MR. Treatment of pemphigus vulgaris with rituximab and intravenous immune globulin. N. Engl. J. Med.355, 1772–1779 (2006).
  • Joly P, Mouquet H, Roujeau JC et al. A single cycle of rituximab for the treatment of severe pemphigus. N. Eng. J. Med.357, 545–552 (2007).
  • Cianchini G, Corona R, Frezzolini A, Ruffelli M, Didona B, Puddu P. Treatment of severe pemphigus with rituximab: report of 12 cases and review of the literature. Arch. Dermatol.143(8), 1033–1038 (2007).
  • Boye J, Elter T, Engert A. An overview of the current clinical use of the anti-CD20 monoclonal antibody rituximab. Ann. Oncol.14, 520–533 (2003).
  • Lehrnbecher T. [Intravenous immunoglobulins in the prevention of infection in children with hematologic–oncologic diseases.] Klin. Padiatr.213(Suppl. 1), A103–A105 (2001).
  • Sullivan KM, Kopecky HJ, Jocom J et al. Immunomodulatory and antimicrobial efficacy of intravenous immunoglobulin in bone marrow transplantation. N. Engl. J. Med.323, 705–712 (1990).
  • Belgi AS, Azeez M, Hoyle C, Willams RE. Anti-CD20 monoclonal antibody (rituximab) in the treatment of pemphigus. Br. J. Dermatol.153, 620–625 (2005).
  • Cooper HL, Healy E, Theaker JM, Friedmann PS. Treatment of resistant pemphigus vulgaris with anti-CD20 monoclonal antibody (rituximab). Clin. Exp. Dermatol.28, 366–368 (2003).
  • Bhol K, Natarajan K, Nagarwalla N, Mohimen A, Aoki V, Ahmed AR. Correlation of peptide specificity and IgG subclass with pathogenic and non-pathogenic autoantibodies in pemphigus vulgaris. Proc. Natl Acad. Sci. USA92, 5239–5243 (1995).
  • Harris DP, Haynes L, Sayles PC et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat. Immunol.6, 475–482 (2006).
  • Hertl M, Veldman C. T cellular autoimmunity against desmogleins in pemphigus, an autoantibody-mediated bullous disorder of the skin. Autoimmun. Rev.2, 278–283 (2003).
  • Schmidt E, Hunzelmann N, Zillikens D, Bröcker EB, Goebeler M. Rituximab in refractory autoimmune bullous diseases. Clin. Exp. Dermatol.31, 503–508 (2006).
  • Skok J, Poudrier J, Gray D. Dendritic cell-derived IL-12 promotes B cell induction of Th2 differentiation: a feedback regulation of Th1 development. J. Immunol.163, 4284–4291 (1999).
  • Camisa C, Helm TN, Liu YC et al. Paraneoplastic pemphigus: a report of three cases including one long term survivor. J. Am. Acad. Dermatol.27, 547–553 (1992).
  • Camisa C, Helm TN. Paraneoplastic pemphigus is a distinct neoplasias-induced autoimmune disease. Arch. Dermatol.129, 883–885 (1993).
  • Tóth GG, van der Meer JB, Jonkman MF. Dexamethasone pulse therapy in pemphigus. J. Eur. Acad. Dermatol. Venereol.16(6), 607–611 (2002).
  • Dega H, Laporte JL, Joly P, Gabarre J, André C. Paraneoplastic pemphigus associated with Hodgkins disease. Br. J. Dermatol.138, 196–198 (1998).
  • Martinez De Pablo MI, Iranzo P, Mascara JM, Llambrich A, Baradad M, Herrero C. Paraneoplastic pemphigus associated with non-Hodgkin B-cell lymphoma and good response to prednisone. Acta Dermatol. Venereol.85, 233–235 (2005).
  • Beutner EH, Pelton S, Hashimoto T et al. A nonfatal case and 2 fatal cases of paraneoplastic pemphigus: can complement indirect immunofluorescent test help to identify fatal ‘group A’ paraneoplastic pemphigus cases? J. Am. Acad. Dermatol.47, 841–851 (2002).
  • Williams JV, Marks JG JR, Billingsley EM. Use of mycophenolate mofetil in the treatment of paraneoplastic pemphigus. Br. J. Dermatol.142, 506–508 (2000).
  • Herzberg MS, Schiffer M, Sullivan J, Stapleton K. Paraneoplastic pemphigus in two patients with B-cell non-Hodgkin’s lymphoma: significant responses to cyclophosphamide and prednisolone. Am. J. Hematol.63, 105–106 (2000).
  • Becker R, Bastian C, Wesselmann U, Karl S, Hamm H, Bröcker EB. Paraneoplastic pemphigus treated with dexamethasone/cyclophosphamide pulse therapy. Eur. J. Dermatol.8, 551–553 (1998).
  • Perniciaro C, Kuechle M, Colón-Otero G, Raymond MG, Spear KL, Pittelkow MR. Paraneoplastic pemphigus: a case of prolonged survival. Mayo Clin. Proc.69, 851–855 (1994).
  • Nanda M, Nanda A, Al-Sabah H, Dvorak R, Alsaleh QA. Paraneoplastic pemphigus in association with B-cell lymphocytic leucemia and hepatitis C: favorable response to intravenous immunoglobulins and prednisolone. Int. J. Dermatol.46, 767–769 (2007).
  • Nousari HC, Brodsky RA, Jones RJ, Grever MR, Anhalt GJ. Immunablative high-dose cyclophosphamide without stem cell rescue in paraneoplastic pemphigus: report of a case and review of this new therapy for severe autoimmune disease. J. Am. Acad. Dermatol.40, 750–754 (1999).
  • Marzano AV, Dassoni F, Caputo R. Treatment of refractory blistering autoimmune diseases with Mycophenolic acid. J. Dermatol. Treat.17, 370–376 (2006).
  • Proby C, Fujii Y, Owaribe K, Nishikawa T, Amagai M. Human autoantibodies against HD1/plectin in paraneoplastic pemphigus. J. Invest. Dermatol.112, 153–156 (1999).
  • Izaki S, Yoshizawa Y, Kitamura K et al. Paraneoplastic pemphigus: potential therapeutic effect of plasmapheresis. Br. J. Dermatol.134, 987–989 (1996).
  • Braess J. Mucocutaneous autoimmune syndrome following fludarabine therapy for low-grade non-Hodgkin’s lymphoma of B-cell type (B-NHL). Ann. Hematol.75, 227–230 (1997).
  • Hohwy T, Bang K, Steiniche T, Anker Peterslund N, D’Amore F. Alemtuzumab-induced remission of both severe paraneoplstic pemphigus and leukaemic bone marrow infiltration in a case of treatment-resistant B-cell chronic lymphocytic leukaemia. Eur. J. Haematol.73, 206–209 (2004).
  • Edwards JC, Szczepanski L, Szechinski J et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med.350, 2572–2581 (2004).
  • Dupuy A, Viguier M, Bédane C et al. Treatment of refractory pemphigus vulgaris with rituximab (anti-CD20 monoclonal antibody). Arch. Dermatol.140, 91–96 (2004).
  • Arzoo K, Sadeghi S, Liebman HA. Treatment of refractory antibody mediated autoimmune disorders with an anti-CD20 monoclonal antibody (rituximab). Ann. Rheum. Dis.61, 922–924 (2002).

Website

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:

Order Reprints Request Corporate Permissions

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:

Request Academic Permissions

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.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.