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Published in: Inflammopharmacology 1/2020

01-02-2020 | Atopic Dermatitis | Original Article

Anti-inflammatory effect of bee venom in phthalic anhydride-induced atopic dermatitis animal model

Authors: Yu Jin Lee, Myung Jin Oh, Dong Hun Lee, Yong Sun Lee, Jiin Lee, Deok-Hyun Kim, Cheol-Hoon Choi, Min Jong Song, Ho Sueb Song, Jin Tae Hong

Published in: Inflammopharmacology | Issue 1/2020

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Abstract

Globally, many people have been affected with atopic dermatitis (AD), a chronic inflammatory skin disease. AD is associated with multiple factors such as genetic, inflammatory, and immune factors. Bee venom (BV) is now widely used for the treatment of several inflammatory diseases. However, its effect on 5% phthalic anhydride (PA)-induced AD has not been reported yet. We investigated the anti-inflammatory and anti-AD effects of BV in a PA-induced animal model of AD. Balb/c mice were treated with topical application of 5% PA to the dorsal skin and ears for induction of AD. After 24 h, BV was applied on the back and ear skin of the mice three times a week for 4 weeks. BV treatment significantly reduced the PA-induced AD clinical score, back and ear epidermal thickness, as well as IgE level and infiltration of immune cells in the skin tissues compared to those of control mice. The levels of inflammatory cytokines in the serum were significantly decreased in BV-treated group compared to PA-treated group. In addition, BV inhibited the expression of iNOS and COX-2 as well as the activation of mitogen-activated protein kinase (MAPK) and NF-ҡB induced by PA in the skin tissues. We also found that BV abrogated the lipopolysaccharide or TNF-α/IFN-γ-induced NO production, expression of iNOS and COX-2, as well as MAPK and NF-ҡB signaling pathway in RAW 264.7 and HaCaT cells. These results suggest that BV may be a potential therapeutic macromolecule for the treatment of AD.
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Literature
go back to reference Ahn S, Siddiqi MH, Aceituno VC et al (2016) Ginsenoside Rg5:Rk1 attenuates TNF-alpha/IFN-gamma-induced production of thymus- and activation-regulated chemokine (TARC/CCL17) and LPS-induced NO production via downregulation of NF-kappaB/p38 MAPK/STAT1 signaling in human keratinocytes and macrophages. Vitro Cell Dev Biol Anim 52:287–295 Ahn S, Siddiqi MH, Aceituno VC et al (2016) Ginsenoside Rg5:Rk1 attenuates TNF-alpha/IFN-gamma-induced production of thymus- and activation-regulated chemokine (TARC/CCL17) and LPS-induced NO production via downregulation of NF-kappaB/p38 MAPK/STAT1 signaling in human keratinocytes and macrophages. Vitro Cell Dev Biol Anim 52:287–295
go back to reference Ban M, Hettich D (2005) Effect of Th2 cytokine antagonist treatments on chemical-induced allergic response in mice. J Appl Toxicol 25:239–247PubMed Ban M, Hettich D (2005) Effect of Th2 cytokine antagonist treatments on chemical-induced allergic response in mice. J Appl Toxicol 25:239–247PubMed
go back to reference Brandt EB, Sivaprasad U (2011) Th2 cytokines and atopic dermatitis. J Clin Cell Immunol 2:2011 Brandt EB, Sivaprasad U (2011) Th2 cytokines and atopic dermatitis. J Clin Cell Immunol 2:2011
go back to reference Brunner PM, Guttman-Yassky E, Leung DY (2017) The immunology of atopic dermatitis and its reversibility with broad-spectrum and targeted therapies. J Allergy Clin Immunol 139:S65–S76PubMedPubMedCentral Brunner PM, Guttman-Yassky E, Leung DY (2017) The immunology of atopic dermatitis and its reversibility with broad-spectrum and targeted therapies. J Allergy Clin Immunol 139:S65–S76PubMedPubMedCentral
go back to reference Chen L, Martinez O, Overbergh L, Mathieu C, Prabhakar BS, Chan LS (2004) Early up-regulation of Th2 cytokines and late surge of Th1 cytokines in an atopic dermatitis model. Clin Exp Immunol 138:375–387PubMedPubMedCentral Chen L, Martinez O, Overbergh L, Mathieu C, Prabhakar BS, Chan LS (2004) Early up-regulation of Th2 cytokines and late surge of Th1 cytokines in an atopic dermatitis model. Clin Exp Immunol 138:375–387PubMedPubMedCentral
go back to reference Choi YY, Kim MH, Lee H, Jo SY, Yang WM (2018) (R)-(+)-pulegone suppresses allergic and inflammation responses on 2,4-dinitrochlorobenzene-induced atopic dermatitis in mice model. J Dermatol Sci 91:292–300PubMed Choi YY, Kim MH, Lee H, Jo SY, Yang WM (2018) (R)-(+)-pulegone suppresses allergic and inflammation responses on 2,4-dinitrochlorobenzene-induced atopic dermatitis in mice model. J Dermatol Sci 91:292–300PubMed
go back to reference Cohen DE, Heidary N (2004) Treatment of irritant and allergic contact dermatitis. Dermatol Ther 17:334–340PubMed Cohen DE, Heidary N (2004) Treatment of irritant and allergic contact dermatitis. Dermatol Ther 17:334–340PubMed
go back to reference Dearman RJ, Kimber I (1992) Divergent immune responses to respiratory and contact chemical allergens: antibody elicited by phthalic anhydride and oxazolone. Clin Exp Allergy 22:241–250PubMed Dearman RJ, Kimber I (1992) Divergent immune responses to respiratory and contact chemical allergens: antibody elicited by phthalic anhydride and oxazolone. Clin Exp Allergy 22:241–250PubMed
go back to reference Friedmann PS (2006) Contact sensitisation and allergic contact dermatitis: immunobiological mechanisms. Toxicol Lett 162:49–54PubMed Friedmann PS (2006) Contact sensitisation and allergic contact dermatitis: immunobiological mechanisms. Toxicol Lett 162:49–54PubMed
go back to reference Han JH, Ju JH, Lee YS et al (2018) Astaxanthin alleviated ethanol-induced liver injury by inhibition of oxidative stress and inflammatory responses via blocking of STAT3 activity. Sci Rep 8:14090PubMedPubMedCentral Han JH, Ju JH, Lee YS et al (2018) Astaxanthin alleviated ethanol-induced liver injury by inhibition of oxidative stress and inflammatory responses via blocking of STAT3 activity. Sci Rep 8:14090PubMedPubMedCentral
go back to reference Hartmann A, Mullner J, Meier N et al (2016) Bee venom for the treatment of Parkinson disease—a randomized controlled clinical trial. PLoS ONE 11:e0158235PubMedPubMedCentral Hartmann A, Mullner J, Meier N et al (2016) Bee venom for the treatment of Parkinson disease—a randomized controlled clinical trial. PLoS ONE 11:e0158235PubMedPubMedCentral
go back to reference Homey B, Steinhoff M, Ruzicka T, Leung DY (2006) Cytokines and chemokines orchestrate atopic skin inflammation. J Allergy Clin Immunol 118:178–189PubMed Homey B, Steinhoff M, Ruzicka T, Leung DY (2006) Cytokines and chemokines orchestrate atopic skin inflammation. J Allergy Clin Immunol 118:178–189PubMed
go back to reference Jeon YD, Kee JY, Kim DS et al (2015) Effects of Ixeris dentata water extract and caffeic acid on allergic inflammation in vivo and in vitro. BMC Complement Altern Med 15:196PubMedPubMedCentral Jeon YD, Kee JY, Kim DS et al (2015) Effects of Ixeris dentata water extract and caffeic acid on allergic inflammation in vivo and in vitro. BMC Complement Altern Med 15:196PubMedPubMedCentral
go back to reference Ju Ho P, Jun Sung J, Ki Cheon K, Jin Tae H (2018) Anti-inflammatory effect of Centella asiatica phytosome in a mouse model of phthalic anhydride-induced atopic dermatitis. Phytomedicine 43:110–119PubMed Ju Ho P, Jun Sung J, Ki Cheon K, Jin Tae H (2018) Anti-inflammatory effect of Centella asiatica phytosome in a mouse model of phthalic anhydride-induced atopic dermatitis. Phytomedicine 43:110–119PubMed
go back to reference Jung M, Choi J, Lee SA, Kim H, Hwang J, Choi EH (2014) Pyrrolidone carboxylic acid levels or caspase-14 expression in the corneocytes of lesional skin correlates with clinical severity, skin barrier function and lesional inflammation in atopic dermatitis. J Dermatol Sci 76:231–239PubMed Jung M, Choi J, Lee SA, Kim H, Hwang J, Choi EH (2014) Pyrrolidone carboxylic acid levels or caspase-14 expression in the corneocytes of lesional skin correlates with clinical severity, skin barrier function and lesional inflammation in atopic dermatitis. J Dermatol Sci 76:231–239PubMed
go back to reference Kim SY, Sohn EJ, Kim DW et al (2011) Transduced PEP-1-FK506BP ameliorates atopic dermatitis in NC/Nga mice. J Invest Dermatol 131:1477–1485PubMed Kim SY, Sohn EJ, Kim DW et al (2011) Transduced PEP-1-FK506BP ameliorates atopic dermatitis in NC/Nga mice. J Invest Dermatol 131:1477–1485PubMed
go back to reference Kim IS, Kim MJ, Shin DH, Son KH, Park HY, Lee JS (2013a) Arazyme inhibits cytokine expression and upregulates skin barrier protein expression. Mol Med Rep 8:551–556PubMed Kim IS, Kim MJ, Shin DH, Son KH, Park HY, Lee JS (2013a) Arazyme inhibits cytokine expression and upregulates skin barrier protein expression. Mol Med Rep 8:551–556PubMed
go back to reference Kim KH, Lee WR, An HJ et al (2013b) Bee venom ameliorates compound 48/80-induced atopic dermatitis-related symptoms. Int J Clin Exp Pathol 6:2896–2903PubMedPubMedCentral Kim KH, Lee WR, An HJ et al (2013b) Bee venom ameliorates compound 48/80-induced atopic dermatitis-related symptoms. Int J Clin Exp Pathol 6:2896–2903PubMedPubMedCentral
go back to reference Kim GD, Lee SE, Park YS, Shin DH, Park GG, Park CS (2014) Immunosuppressive effects of fisetin against dinitrofluorobenzene-induced atopic dermatitis-like symptoms in NC/Nga mice. Food Chem Toxicol 66:341–349PubMed Kim GD, Lee SE, Park YS, Shin DH, Park GG, Park CS (2014) Immunosuppressive effects of fisetin against dinitrofluorobenzene-induced atopic dermatitis-like symptoms in NC/Nga mice. Food Chem Toxicol 66:341–349PubMed
go back to reference Lee JD, Kim SY, Kim TW et al (2004) Anti-inflammatory effect of bee venom on type II collagen-induced arthritis. Am J Chin Med 32:361–367PubMed Lee JD, Kim SY, Kim TW et al (2004) Anti-inflammatory effect of bee venom on type II collagen-induced arthritis. Am J Chin Med 32:361–367PubMed
go back to reference Lee YJ, Kim JE, Kwak MH et al (2014) Quantitative evaluation of the therapeutic effect of fermented soybean products containing a high concentration of GABA on phthalic anhydride-induced atopic dermatitis in IL-4/Luc/CNS-1 Tg mice. Int J Mol Med 33:1185–1194PubMed Lee YJ, Kim JE, Kwak MH et al (2014) Quantitative evaluation of the therapeutic effect of fermented soybean products containing a high concentration of GABA on phthalic anhydride-induced atopic dermatitis in IL-4/Luc/CNS-1 Tg mice. Int J Mol Med 33:1185–1194PubMed
go back to reference Lee HJ, Kim MH, Choi YY et al (2016) Improvement of atopic dermatitis with topical application of Spirodela polyrhiza. J Ethnopharmacol 180:12–17PubMed Lee HJ, Kim MH, Choi YY et al (2016) Improvement of atopic dermatitis with topical application of Spirodela polyrhiza. J Ethnopharmacol 180:12–17PubMed
go back to reference Lee DY, Hwang CJ, Choi JY et al (2017) Inhibitory effect of carnosol on phthalic anhydride-induced atopic dermatitis via inhibition of STAT3. Biomol Ther (Seoul) 25:535–544PubMedCentral Lee DY, Hwang CJ, Choi JY et al (2017) Inhibitory effect of carnosol on phthalic anhydride-induced atopic dermatitis via inhibition of STAT3. Biomol Ther (Seoul) 25:535–544PubMedCentral
go back to reference Lee YS, Lee CH, Bae JT et al (2018) Inhibition of skin carcinogenesis by suppression of NF-κB dependent ITGAV and TIMP-1 expression in IL-32γ overexpressed condition. J Exp Clin Cancer Res 37:293PubMedPubMedCentral Lee YS, Lee CH, Bae JT et al (2018) Inhibition of skin carcinogenesis by suppression of NF-κB dependent ITGAV and TIMP-1 expression in IL-32γ overexpressed condition. J Exp Clin Cancer Res 37:293PubMedPubMedCentral
go back to reference Leung DY (2000) Atopic dermatitis: new insights and opportunities for therapeutic intervention. J Allergy Clin Immunol 105:860–876PubMed Leung DY (2000) Atopic dermatitis: new insights and opportunities for therapeutic intervention. J Allergy Clin Immunol 105:860–876PubMed
go back to reference Li C, Maillet I, Mackowiak C et al (2017) Experimental atopic dermatitis depends on IL-33R signaling via MyD88 in dendritic cells. Cell Death Dis 8:e2735PubMedPubMedCentral Li C, Maillet I, Mackowiak C et al (2017) Experimental atopic dermatitis depends on IL-33R signaling via MyD88 in dendritic cells. Cell Death Dis 8:e2735PubMedPubMedCentral
go back to reference Lim JM, Lee B, Min JH et al (2018) Effect of peiminine on DNCB-induced atopic dermatitis by inhibiting inflammatory cytokine expression in vivo and in vitro. Int Immunopharmacol 56:135–142PubMed Lim JM, Lee B, Min JH et al (2018) Effect of peiminine on DNCB-induced atopic dermatitis by inhibiting inflammatory cytokine expression in vivo and in vitro. Int Immunopharmacol 56:135–142PubMed
go back to reference Man G, Hu LZ, Elias PM, Man MQ (2018) Therapeutic benefits of natural ingredients for atopic dermatitis. Chin J Integr Med 24:308–314PubMed Man G, Hu LZ, Elias PM, Man MQ (2018) Therapeutic benefits of natural ingredients for atopic dermatitis. Chin J Integr Med 24:308–314PubMed
go back to reference Neis MM, Peters B, Dreuw A et al (2006) Enhanced expression levels of IL-31 correlate with IL-4 and IL-13 in atopic and allergic contact dermatitis. J Allergy Clin Immunol 118:930–937PubMed Neis MM, Peters B, Dreuw A et al (2006) Enhanced expression levels of IL-31 correlate with IL-4 and IL-13 in atopic and allergic contact dermatitis. J Allergy Clin Immunol 118:930–937PubMed
go back to reference Ozturk AB, Bayraktar R, Gogebakan B, Mumbuc S, Bayram H (2017) Comparison of inflammatory cytokine release from nasal epithelial cells of non-atopic non-rhinitic, allergic rhinitic and polyp subjects and effects of diesel exhaust particles in vitro. Allergol Immunopathol (Madr) 45:473–481 Ozturk AB, Bayraktar R, Gogebakan B, Mumbuc S, Bayram H (2017) Comparison of inflammatory cytokine release from nasal epithelial cells of non-atopic non-rhinitic, allergic rhinitic and polyp subjects and effects of diesel exhaust particles in vitro. Allergol Immunopathol (Madr) 45:473–481
go back to reference Park SJ, Lee YH, Lee KH, Kim TJ (2013) Effect of eriodictyol on the development of atopic dermatitis-like lesions in ICR mice. Biol Pharm Bull 36:1375–1379PubMed Park SJ, Lee YH, Lee KH, Kim TJ (2013) Effect of eriodictyol on the development of atopic dermatitis-like lesions in ICR mice. Biol Pharm Bull 36:1375–1379PubMed
go back to reference Park JH, Kim MS, Jeong GS, Yoon J (2015) Xanthii fructus extract inhibits TNF-alpha/IFN-gamma-induced Th2-chemokines production via blockade of NF-kappaB, STAT1 and p38-MAPK activation in human epidermal keratinocytes. J Ethnopharmacol 171:85–93PubMed Park JH, Kim MS, Jeong GS, Yoon J (2015) Xanthii fructus extract inhibits TNF-alpha/IFN-gamma-induced Th2-chemokines production via blockade of NF-kappaB, STAT1 and p38-MAPK activation in human epidermal keratinocytes. J Ethnopharmacol 171:85–93PubMed
go back to reference Schakel K, Dobel T, Bosselmann I (2014) Future treatment options for atopic dermatitis—small molecules and beyond. J Dermatol Sci 73:91–100PubMed Schakel K, Dobel T, Bosselmann I (2014) Future treatment options for atopic dermatitis—small molecules and beyond. J Dermatol Sci 73:91–100PubMed
go back to reference Schreiber S, Kilgus O, Payer E et al (1992) Cytokine pattern of Langerhans cells isolated from murine epidermal cell cultures. J Immunol 149:3524–3534PubMed Schreiber S, Kilgus O, Payer E et al (1992) Cytokine pattern of Langerhans cells isolated from murine epidermal cell cultures. J Immunol 149:3524–3534PubMed
go back to reference Seo WY, Youn GS, Choi SY, Park J (2015) Butein, a tetrahydroxychalcone, suppresses pro-inflammatory responses in HaCaT keratinocytes. BMB Rep 48:495–500PubMedPubMedCentral Seo WY, Youn GS, Choi SY, Park J (2015) Butein, a tetrahydroxychalcone, suppresses pro-inflammatory responses in HaCaT keratinocytes. BMB Rep 48:495–500PubMedPubMedCentral
go back to reference Sredni-Kenigsbuch D, Shohat M, Shohat B, Ben-Amitai D, Chan CC, David M (2008) The novel tellurium immunomodulator AS101 inhibits interleukin-10 production and p38 MAPK expression in atopic dermatitis. J Dermatol Sci 50:232–235PubMed Sredni-Kenigsbuch D, Shohat M, Shohat B, Ben-Amitai D, Chan CC, David M (2008) The novel tellurium immunomodulator AS101 inhibits interleukin-10 production and p38 MAPK expression in atopic dermatitis. J Dermatol Sci 50:232–235PubMed
go back to reference Suh SJ, Kim KS, Kim MJ et al (2006) Effects of bee venom on protease activities and free radical damages in synovial fluid from type II collagen-induced rheumatoid arthritis rats. Toxicol In Vitro 20:1465–1471PubMed Suh SJ, Kim KS, Kim MJ et al (2006) Effects of bee venom on protease activities and free radical damages in synovial fluid from type II collagen-induced rheumatoid arthritis rats. Toxicol In Vitro 20:1465–1471PubMed
go back to reference Sun M, Wang S, Zhao L et al (2014) Suppression of 2,4-dinitrochlorobenzene-induced atopic dermatitis by extract of Bacillus Calmette–Guerin. Mol Med Rep 9:689–694PubMed Sun M, Wang S, Zhao L et al (2014) Suppression of 2,4-dinitrochlorobenzene-induced atopic dermatitis by extract of Bacillus Calmette–Guerin. Mol Med Rep 9:689–694PubMed
go back to reference Sur B, Lee B, Yeom M et al (2016) Bee venom acupuncture alleviates trimellitic anhydride-induced atopic dermatitis-like skin lesions in mice. BMC Complement Altern Med 16:38PubMedPubMedCentral Sur B, Lee B, Yeom M et al (2016) Bee venom acupuncture alleviates trimellitic anhydride-induced atopic dermatitis-like skin lesions in mice. BMC Complement Altern Med 16:38PubMedPubMedCentral
go back to reference Suzuki H, Makino Y, Nagata M et al (2016) A rare variant in CYP27A1 and its association with atopic dermatitis with high serum total IgE. Allergy 71:1486–1489PubMed Suzuki H, Makino Y, Nagata M et al (2016) A rare variant in CYP27A1 and its association with atopic dermatitis with high serum total IgE. Allergy 71:1486–1489PubMed
go back to reference Tan HY, Zhang AL, Chen D, Xue CC, Lenon GB (2013) Chinese herbal medicine for atopic dermatitis: a systematic review. J Am Acad Dermatol 69:295–304PubMed Tan HY, Zhang AL, Chen D, Xue CC, Lenon GB (2013) Chinese herbal medicine for atopic dermatitis: a systematic review. J Am Acad Dermatol 69:295–304PubMed
go back to reference Tanaka A, Konno M, Muto S et al (2005) A novel NF-kappaB inhibitor, IMD-0354, suppresses neoplastic proliferation of human mast cells with constitutively activated c-kit receptors. Blood 105:2324–2331PubMed Tanaka A, Konno M, Muto S et al (2005) A novel NF-kappaB inhibitor, IMD-0354, suppresses neoplastic proliferation of human mast cells with constitutively activated c-kit receptors. Blood 105:2324–2331PubMed
go back to reference Tanaka A, Muto S, Jung K, Itai A, Matsuda H (2007) Topical application with a new NF-kappaB inhibitor improves atopic dermatitis in NC/NgaTnd mice. J Invest Dermatol 127:855–863PubMed Tanaka A, Muto S, Jung K, Itai A, Matsuda H (2007) Topical application with a new NF-kappaB inhibitor improves atopic dermatitis in NC/NgaTnd mice. J Invest Dermatol 127:855–863PubMed
go back to reference Tokura Y (2010) Extrinsic and intrinsic types of atopic dermatitis. J Dermatol Sci 58:1–7PubMed Tokura Y (2010) Extrinsic and intrinsic types of atopic dermatitis. J Dermatol Sci 58:1–7PubMed
go back to reference Wullaert A, Bonnet MC, Pasparakis M (2011) NF-kappaB in the regulation of epithelial homeostasis and inflammation. Cell Res 21:146–158PubMed Wullaert A, Bonnet MC, Pasparakis M (2011) NF-kappaB in the regulation of epithelial homeostasis and inflammation. Cell Res 21:146–158PubMed
go back to reference Yamashita H, Tanaka H, Inagaki N (2013) Treatment of the chronic itch of atopic dermatitis using standard drugs and kampo medicines. Biol Pharm Bull 36:1253–1257PubMed Yamashita H, Tanaka H, Inagaki N (2013) Treatment of the chronic itch of atopic dermatitis using standard drugs and kampo medicines. Biol Pharm Bull 36:1253–1257PubMed
go back to reference Yanashima K, Chieosilapatham P, Yoshimoto E, Okumura K, Ogawa H, Niyonsaba F (2017) Innate defense regulator IDR-1018 activates human mast cells through G protein-, phospholipase C-, MAPK- and NF-kB-sensitive pathways. Immunol Res 65:920–931PubMed Yanashima K, Chieosilapatham P, Yoshimoto E, Okumura K, Ogawa H, Niyonsaba F (2017) Innate defense regulator IDR-1018 activates human mast cells through G protein-, phospholipase C-, MAPK- and NF-kB-sensitive pathways. Immunol Res 65:920–931PubMed
go back to reference Yang G, Choi CH, Lee K, Lee M, Ham I, Choi HY (2013) Effects of Catalpa ovata stem bark on atopic dermatitis-like skin lesions in NC/Nga mice. J Ethnopharmacol 145:416–423PubMed Yang G, Choi CH, Lee K, Lee M, Ham I, Choi HY (2013) Effects of Catalpa ovata stem bark on atopic dermatitis-like skin lesions in NC/Nga mice. J Ethnopharmacol 145:416–423PubMed
go back to reference Zhang S, Liu Y, Ye Y et al (2018) Bee venom therapy: potential mechanisms and therapeutic applications. Toxicon 148:64–73PubMed Zhang S, Liu Y, Ye Y et al (2018) Bee venom therapy: potential mechanisms and therapeutic applications. Toxicon 148:64–73PubMed
Metadata
Title
Anti-inflammatory effect of bee venom in phthalic anhydride-induced atopic dermatitis animal model
Authors
Yu Jin Lee
Myung Jin Oh
Dong Hun Lee
Yong Sun Lee
Jiin Lee
Deok-Hyun Kim
Cheol-Hoon Choi
Min Jong Song
Ho Sueb Song
Jin Tae Hong
Publication date
01-02-2020
Publisher
Springer International Publishing
Published in
Inflammopharmacology / Issue 1/2020
Print ISSN: 0925-4692
Electronic ISSN: 1568-5608
DOI
https://doi.org/10.1007/s10787-019-00646-w

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