Abstract
Purpose
Although the dismal clinical prognosis of diffuse intrinsic pontine glioma (DIPG) has not changed, there has been significant progress in the academic literature made in the biological understanding of this brainstem tumor. The aim of this analysis was to evaluate citation and other bibliometric characteristics of the 100 most-cited DIPG articles in the current literature in order to better understand the current state of our academic efforts in this area.
Methods
Elsevier’s Scopus database was searched for the 100 most-cited articles that focussed on DIPG. Articles were dichotomized as either primarily basic science (BSc) or clinical (CL) articles. Various bibliometric parameters were summarized and comparison between BSc and CL articles was performed using Pearson’s chi-square and Mann–Whitney U tests.
Results
Of the 100 most-cited articles, 36 (36%) were BSc and 64 (64%) were CL articles. Overall median values were as follows: citation count, 52 (range, 27–261); citation rate per year, 8.6 (range, 1.7–104); number of authors, 9 (range, 1–63); and publication year, 2011 (range, 1997–2017). Articles were published in a total of 43 different journals and predominately originated in the USA (n = 67, 67%). When compared with CL articles, BSc articles reported significantly greater citation count (P = 0.03), citations rate per year (P < 0.01), number of authors (P < 0.01), and more recent years of publication (P < 0.01).
Conclusions
The 100 most-cited articles about DIPG were characterized in this analysis. Although smaller in overall proportion, BSc articles demonstrated significantly increased bibliometric parameters, supporting the recent dominance of BSc in this field, primarily involving histone biology of the H3K27M mutation. Moving forward, it will be of great interest to see how the findings of these high-impact BSc articles will translate into future high-impact CL articles.
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References
Bender S, Tang Y, Lindroth AM, Hovestadt V, Jones DT, Kool M, Zapatka M, Northcott PA, Sturm D, Wang W, Radlwimmer B, Hojfeldt JW, Truffaux N, Castel D, Schubert S, Ryzhova M, Seker-Cin H, Gronych J, Johann PD, Stark S, Meyer J, Milde T, Schuhmann M, Ebinger M, Monoranu CM, Ponnuswami A, Chen S, Jones C, Witt O, Collins VP, von Deimling A, Jabado N, Puget S, Grill J, Helin K, Korshunov A, Lichter P, Monje M, Plass C, Cho YJ, Pfister SM (2013) Reduced H3K27me3 and DNA hypomethylation are major drivers of gene expression in K27M mutant pediatric high-grade gliomas. Cancer Cell 24:660–672. https://doi.org/10.1016/j.ccr.2013.10.006
Buczkowicz P, Bartels U, Bouffet E, Becher O, Hawkins C (2014) Histopathological spectrum of paediatric diffuse intrinsic pontine glioma: diagnostic and therapeutic implications. Acta Neuropathol 128:573–581. https://doi.org/10.1007/s00401-014-1319-6
Buczkowicz P, Hawkins C (2015) Pathology, molecular genetics, and epigenetics of diffuse intrinsic pontine glioma. Front Oncol 5:147. https://doi.org/10.3389/fonc.2015.00147
Buczkowicz P, Hoeman C, Rakopoulos P, Pajovic S, Letourneau L, Dzamba M, Morrison A, Lewis P, Bouffet E, Bartels U, Zuccaro J, Agnihotri S, Ryall S, Barszczyk M, Chornenkyy Y, Bourgey M, Bourque G, Montpetit A, Cordero F, Castelo-Branco P, Mangerel J, Tabori U, Ho KC, Huang A, Taylor KR, Mackay A, Bendel AE, Nazarian J, Fangusaro JR, Karajannis MA, Zagzag D, Foreman NK, Donson A, Hegert JV, Smith A, Chan J, Lafay-Cousin L, Dunn S, Hukin J, Dunham C, Scheinemann K, Michaud J, Zelcer S, Ramsay D, Cain J, Brennan C, Souweidane MM, Jones C, Allis CD, Brudno M, Becher O, Hawkins C (2014) Genomic analysis of diffuse intrinsic pontine gliomas identifies three molecular subgroups and recurrent activating ACVR1 mutations. Nat Genet 46:451–456. https://doi.org/10.1038/ng.2936
Castel D, Philippe C, Calmon R, Le Dret L, Truffaux N, Boddaert N, Pagès M, Taylor KR, Saulnier P, Lacroix L, Mackay A, Jones C, Sainte-Rose C, Blauwblomme T, Andreiuolo F, Puget S, Grill J, Varlet P, Debily MA (2015) Histone H3F3A and HIST1H3B K27M mutations define two subgroups of diffuse intrinsic pontine gliomas with different prognosis and phenotypes. Acta Neuropathol 130:815–827. https://doi.org/10.1007/s00401-015-1478-0
Chan KM, Fang D, Gan H, Hashizume R, Yu C, Schroeder M, Gupta N, Mueller S, David James C, Jenkins R, Sarkaria J, Zhang Z (2013) The histone H3.3K27M mutation in pediatric glioma reprograms H3K27 methylation and gene expression. Genes Dev 27:985–990. https://doi.org/10.1101/gad.217778.113
Falagas ME, Pitsouni EI, Malietzis GA, Pappas G (2008) Comparison of PubMed, Scopus, web of science, and Google scholar: strengths and weaknesses. FASEB J 22:338–342
Grasso CS, Tang Y, Truffaux N, Berlow NE, Liu L, Debily MA, Quist MJ, Davis LE, Huang EC, Woo PJ, Ponnuswami A, Chen S, Johung TB, Sun W, Kogiso M, Du Y, Qi L, Huang Y, Hütt-Cabezas M, Warren KE, Le Dret L, Meltzer PS, Mao H, Quezado M, Van Vuurden DG, Abraham J, Fouladi M, Svalina MN, Wang N, Hawkins C, Nazarian J, Alonso MM, Raabe EH, Hulleman E, Spellman PT, Li XN, Keller C, Pal R, Grill J, Monje M (2015) Functionally defined therapeutic targets in diffuse intrinsic pontine glioma. Nat Med 21:555–559. https://doi.org/10.1038/nm.3855
Grill J, Puget S, Andreiuolo F, Philippe C, MacConaill L, Kieran MW (2012) Critical oncogenic mutations in newly diagnosed pediatric diffuse intrinsic pontine glioma. Pediatr Blood Cancer 58:489–491. https://doi.org/10.1002/pbc.24060
Gupta N, Goumnerova LC, Manley P, Chi SN, Neuberg D, Puligandla M, Fangusaro J, Goldman S, Tomita T, Alden T, Dipatri A, Rubin JB, Gauvain K, Limbrick D, Leonard J, Geyer JR, Leary S, Browd S, Wang Z, Sood S, Bendel A, Nagib M, Gardner S, Karajannis MA, Harter D, Ayyanar K, Gump W, Bowers DC, Weprin B, Macdonald TJ, Aguilera D, Brahma B, Robison NJ, Kiehna E, Krieger M, Sandler E, Aldana P, Khatib Z, Ragheb J, Bhatia S, Mueller S, Banerjee A, Bredlau AL, Gururangan S, Fuchs H, Cohen KJ, Jallo G, Dorris K, Handler M, Comito M, Dias M, Nazemi K, Baird L, Murray J, Lindeman N, Hornick JL, Malkin H, Sinai C, Greenspan L, Wright KD, Prados M, Bandopadhayay P, Ligon KL, Kieran MW (2018) Prospective feasibility and safety assessment of surgical biopsy for patients with newly diagnosed diffuse intrinsic pontine glioma. Neuro-Oncology 20:1547–1555. https://doi.org/10.1093/neuonc/noy070
Hargrave D, Bartels U, Bouffet E (2006) Diffuse brainstem glioma in children: critical review of clinical trials. Lancet Oncol 7:241–248. https://doi.org/10.1016/S1470-2045(06)70615-5
Himes BT, Zhang L, Daniels DJ (2019) Treatment strategies in diffuse midline gliomas with the H3K27M mutation: the role of convection-enhanced delivery in overcoming anatomic challenges. Front Oncol 9:31. https://doi.org/10.3389/fonc.2019.00031
Hoeman CM, Cordero FJ, Hu G, Misuraca K, Romero MM, Cardona HJ, Nazarian J, Hashizume R, McLendon R, Yu P, Procissi D, Gadd S, Becher OJ (2019) ACVR1 R206H cooperates with H3.1K27M in promoting diffuse intrinsic pontine glioma pathogenesis. Nat Commun 10:1023. https://doi.org/10.1038/s41467-019-08823-9
Huang TY, Piunti A, Lulla RR, Qi J, Horbinski CM, Tomita T, James CD, Shilatifard A, Saratsis AM (2017) Detection of histone H3 mutations in cerebrospinal fluid-derived tumor DNA from children with diffuse midline glioma. Acta Neuropathologica Communications 5:28. https://doi.org/10.1186/s40478-017-0436-6
Jalali R, Raut N, Arora B, Gupta T, Dutta D, Munshi A, Sarin R, Kurkure P (2010) Prospective evaluation of radiotherapy with concurrent and adjuvant temozolomide in children with newly diagnosed diffuse intrinsic pontine glioma. Int J Radiat Oncol Biol Phys 77:113–118. https://doi.org/10.1016/j.ijrobp.2009.04.031
Jansen MH, Van Zanten SEV, Aliaga ES, Heymans MW, Warmuth-Metz M, Hargrave D, Van Der Hoeven EJ, Gidding CE, De Bont ES, Eshghi OS, Reddingius R, Peeters CM, Schouten-Van Meeteren AYN, Gooskens RHJ, Granzen B, Paardekooper GM, Janssens GO, Noske DP, Barkhof F, Kramm CM, Vandertop WP, Kaspers GJ, Van Vuurden DG (2015) Survival prediction model of children with diffuse intrinsic pontine glioma based on clinical and radiological criteria. Neuro-Oncology 17:160–166. https://doi.org/10.1093/neuonc/nou104
Jones C, Baker SJ (2014) Unique genetic and epigenetic mechanisms driving paediatric diffuse high-grade glioma. Nat Rev Cancer 14:651–661. https://doi.org/10.1038/nrc3811
Khuong-Quang DA, Buczkowicz P, Rakopoulos P, Liu XY, Fontebasso AM, Bouffet E, Bartels U, Albrecht S, Schwartzentruber J, Letourneau L, Bourgey M, Bourque G, Montpetit A, Bourret G, Lepage P, Fleming A, Lichter P, Kool M, Von Deimling A, Sturm D, Korshunov A, Faury D, Jones DT, Majewski J, Pfister SM, Jabado N, Hawkins C (2012) K27M mutation in histone H3.3 defines clinically and biologically distinct subgroups of pediatric diffuse intrinsic pontine gliomas. Acta Neuropathol 124:439–447. https://doi.org/10.1007/s00401-012-0998-0
Lewis PW, Müller MM, Koletsky MS, Cordero F, Lin S, Banaszynski LA, Garcia BA, Muir TW, Becher OJ, Allis CD (2013) Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 340:857–861. https://doi.org/10.1126/science.1232245
Lim KJ, Yoon DY, Yun EJ, Seo YL, Baek S, Gu DH, Yoon SJ, Han A, Ku YJ, Kim SSJR (2012) Characteristics and trends of radiology research: a survey of original articles published in AJR and radiology between 2001 and 2010. Radiology 264:796–802
Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (2016) WHO classification of tumours of the central nervous system, revised. fourth edition. IARC Press, Lyon
Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131:803–820. https://doi.org/10.1007/s00401-016-1545-1
Mackay A, Burford A, Carvalho D, Izquierdo E, Fazal-Salom J, Taylor KR, Bjerke L, Clarke M, Vinci M, Nandhabalan M, Temelso S, Popov S, Molinari V, Raman P, Waanders AJ, Han HJ, Gupta S, Marshall L, Zacharoulis S, Vaidya S, Mandeville HC, Bridges LR, Martin AJ, Al-Sarraj S, Chandler C, Ng HK, Li X, Mu K, Trabelsi S, Brahim DHB, Kisljakov AN, Konovalov DM, Moore AS, Carcaboso AM, Sunol M, de Torres C, Cruz O, Mora J, Shats LI, Stavale JN, Bidinotto LT, Reis RM, Entz-Werle N, Farrell M, Cryan J, Crimmins D, Caird J, Pears J, Monje M, Debily MA, Castel D, Grill J, Hawkins C, Nikbakht H, Jabado N, Baker SJ, Pfister SM, Jones DTW, Fouladi M, von Bueren AO, Baudis M, Resnick A, Jones C (2017) Integrated molecular meta-analysis of 1,000 pediatric high-grade and diffuse intrinsic pontine glioma. Cancer Cell 32:520–537.e525. https://doi.org/10.1016/j.ccell.2017.08.017
Mandell LR, Kadota R, Freeman C, Douglass EC, Fontanesi J, Cohen ME, Kovnar E, Burger P, Sanford RA, Kepner J, Friedman H, Kun LE (1999) There is no role for hyperfractionated radiotherapy in the management of children with newly diagnosed diffuse intrinsic brainstem tumors: results of a pediatric oncology group phase III trial comparing conventional vs. hyperfractionated radiotherapy. Int J Radiat Oncol Biol Phys 43:959–964. https://doi.org/10.1016/S0360-3016(98)00501-X
Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, Gnirke A, Jaenisch R, Lander ES (2008) Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454:766–770. https://doi.org/10.1038/nature07107
Merchant TE, Pollack IF, Loeffler JS (2010) Brain tumors across the age spectrum: biology, therapy, and late effects. Semin Radiat Oncol 20:58–66. https://doi.org/10.1016/j.semradonc.2009.09.005
Nikbakht H, Panditharatna E, Mikael LG, Li R, Gayden T, Osmond M, Ho CY, Kambhampati M, Hwang EI, Faury D, Siu A, Papillon-Cavanagh S, Bechet D, Ligon KL, Ellezam B, Ingram WJ, Stinson C, Moore AS, Warren KE, Karamchandani J, Packer RJ, Jabado N, Majewski J, Nazarian J (2016) Spatial and temporal homogeneity of driver mutations in diffuse intrinsic pontine glioma. Nat Commun 7:11185. https://doi.org/10.1038/ncomms11185
Ostrom QT, Gittleman H, Truitt G, Boscia A, Kruchko C, Barnholtz-Sloan JS (2018) CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2011–2015. Neuro-Oncology 20:iv1–iv86. https://doi.org/10.1093/neuonc/noy131
Pan C, Diplas BH, Chen X, Wu Y, Xiao X, Jiang L, Geng Y, Xu C, Sun Y, Zhang P, Wu W, Wang Y, Wu Z, Zhang J, Jiao Y, Yan H, Zhang L (2019) Molecular profiling of tumors of the brainstem by sequencing of CSF-derived circulating tumor DNA. Acta Neuropathol 137:297–306. https://doi.org/10.1007/s00401-018-1936-6
Paugh BS, Broniscer A, Qu C, Miller CP, Zhang J, Tatevossian RG, Olson JM, Geyer JR, Chi SN, Da Silva NS, Onar-Thomas A, Baker JN, Gajjar A, Ellison DW, Baker SJ (2011) Genome-wide analyses identify recurrent amplifications of receptor tyrosine kinases and cell-cycle regulatory genes in diffuse intrinsic pontine glioma. J Clin Oncol 29:3999–4006. https://doi.org/10.1200/JCO.2011.35.5677
Paugh BS, Qu C, Jones C, Liu Z, Adamowicz-Brice M, Zhang J, Bax DA, Coyle B, Barrow J, Hargrave D, Lowe J, Gajjar A, Zhao W, Broniscer A, Ellison DW, Grundy RG, Baker SJ (2010) Integrated molecular genetic profiling of pediatric high-grade gliomas reveals key differences with the adult disease. J Clin Oncol 28:3061–3068. https://doi.org/10.1200/JCO.2009.26.7252
Paugh BS, Zhu X, Qu C, Endersby R, Diaz AK, Zhang J, Bax DA, Carvalho D, Reis RM, Onar-Thomas A, Broniscer A, Wetmore C, Zhang J, Jones C, Ellison DW, Baker SJ (2013) Novel oncogenic PDGFRA mutations in pediatric high-grade gliomas. Cancer Res 73:6219–6229. https://doi.org/10.1158/0008-5472.CAN-13-1491
Puget S, Beccaria K, Blauwblomme T, Roujeau T, James S, Grill J, Zerah M, Varlet P, Sainte-Rose C (2015) Biopsy in a series of 130 pediatric diffuse intrinsic Pontine gliomas. Childs Nerv Syst 31:1773–1780. https://doi.org/10.1007/s00381-015-2832-1
Reynolds N, Salmon-Divon M, Dvinge H, Hynes-Allen A, Balasooriya G, Leaford D, Behrens A, Bertone P, Hendrich B (2012) NuRD-mediated deacetylation of H3K27 facilitates recruitment of polycomb repressive complex 2 to direct gene repression. EMBO J 31:593–605. https://doi.org/10.1038/emboj.2011.431
Singleton WGB, Bieneman AS, Woolley M, Johnson D, Lewis O, Wyatt MJ, Damment SJP, Boulter LJ, Killick-Cole CL, Asby DJ, Gill SS (2018) The distribution, clearance, and brainstem toxicity of panobinostat administered by convection-enhanced delivery. J Neurosurg Pediatr 22:288–296. https://doi.org/10.3171/2018.2.PEDS17663
Vanan MI, Eisenstat DD (2015) DIPG in children - what can we learn from the past? Front Oncol 5:237. https://doi.org/10.3389/fonc.2015.00237
Veldhuijzen van Zanten SE, Baugh J, Chaney B, De Jongh D, Sanchez Aliaga E, Barkhof F, Noltes J, De Wolf R, Van Dijk J, Cannarozzo A, Damen-Korbijn CM, Lieverst JA, Colditz N, Hoffmann M, Warmuth-Metz M, Bison B, Jones DT, Sturm D, Gielen GH, Jones C, Hulleman E, Calmon R, Castel D, Varlet P, Giraud G, Slavc I, Van Gool S, Jacobs S, Jadrijevic-Cvrlje F, Sumerauer D, Nysom K, Pentikainen V, Kivivuori SM, Leblond P, Entz-Werle N, von Bueren AO, Kattamis A, Hargrave DR, Hauser P, Garami M, Thorarinsdottir HK, Pears J, Gandola L, Rutkauskiene G, Janssens GO, Torsvik IK, Perek-Polnik M, Gil-da-Costa MJ, Zheludkova O, Shats L, Deak L, Kitanovski L, Cruz O, Morales La Madrid A, Holm S, Gerber N, Kebudi R, Grundy R, Lopez-Aguilar E, Zapata-Tarres M, Emmerik J, Hayden T, Bailey S, Biassoni V, Massimino M, Grill J, Vandertop WP, Kaspers GJ, Fouladi M, Kramm CM, van Vuurden DG (2017) Development of the SIOPE DIPG network, registry and imaging repository: a collaborative effort to optimize research into a rare and lethal disease. J Neuro-Oncol 132:255–266. https://doi.org/10.1007/s11060-016-2363-y
Venneti S, Garimella MT, Sullivan LM, Martinez D, Huse JT, Heguy A, Santi M, Thompson CB, Judkins AR (2013) Evaluation of histone 3 lysine 27 trimethylation (H3K27me3) and enhancer of Zest 2 (EZH2) in pediatric glial and glioneuronal tumors shows decreased H3K27me3 in H3F3A K27M mutant glioblastomas. Brain Pathol (Zurich, Switzerland) 23:558–564. https://doi.org/10.1111/bpa.12042
Wu G, Broniscer A, McEachron TA, Lu C, Paugh BS, Becksfort J, Qu C, Ding L, Huether R, Parker M, Zhang J, Gajjar A, Dyer MA, Mullighan CG, Gilbertson RJ, Mardis ER, Wilson RK, Downing JR, Ellison DW, Zhang J, Baker SJ (2012) Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet 44:251–253. https://doi.org/10.1038/ng.1102
Wu G, Diaz AK, Paugh BS, Rankin SL, Ju B, Li Y, Zhu X, Qu C, Chen X, Zhang J, Easton J, Edmonson M, Ma X, Lu C, Nagahawatte P, Hedlund E, Rusch M, Pounds S, Lin T, Onar-Thomas A, Huether R, Kriwacki R, Parker M, Gupta P, Becksfort J, Wei L, Mulder HL, Boggs K, Vadodaria B, Yergeau D, Russell JC, Ochoa K, Fulton RS, Fulton LL, Jones C, Boop FA, Broniscer A, Wetmore C, Gajjar A, Ding L, Mardis ER, Wilson RK, Taylor MR, Downing JR, Ellison DW, Zhang J, Baker SJ (2014) The genomic landscape of diffuse intrinsic pontine glioma and pediatric non-brainstem high-grade glioma. Nat Genet 46:444–450. https://doi.org/10.1038/ng.2938
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EAP was supported by CTSA Grant Number UL1 TR002377 from the National Center for Advancing Translational Sciences (NCATS).
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Lu, V.M., Power, E.A., Kerezoudis, P. et al. The 100 most-cited articles about diffuse intrinsic pontine glioma: a bibliometric analysis. Childs Nerv Syst 35, 2339–2346 (2019). https://doi.org/10.1007/s00381-019-04254-5
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DOI: https://doi.org/10.1007/s00381-019-04254-5