Emerging trends and new developments in regenerative medicine: a scientometric update (2000 – 2014)

Figures & data

Figure 1. A lightweight survey of major topics on the Internet on regenerative medicine is shown. The visualizations were generated by the Carrot system based on first 100 results of search on regenerative medicine. Left: search results from the web. Right: search results from the PubMed.

Table 1. A summary of the datasets collected.

Dataset	Collection	Duration	Results	Articles	Reviews	References	Keywords	Authors	Institutions
DA	Topic search	2000 – 2011	4331	2853	1235	267,545	62,028	21,594	11,712
DB	Citation expanded	2000 – 2014	67,421	52,490	13,056	4,243,303	965,899	389,534	199,613
DC	Topic search	2012 – 2014	2626	1901	670	169,097	38,127	14,969	7963
DD	Citation expanded	2012 – 2014	5069	3805	1208	361,782	72,473	29,377	15,690
DABCD	Combined	2000 – 2014	71,393	61,049	16,169	5,041,714	1,138,527	455,474	234,978

Figure 2. The research fronts and the intellectual base of regenerative medicine are shown. Red dots in the foreground represent research front articles of the D_ABCD dataset (2000 – 2014). A total of 34,805 dots of various other colors in the background represent references that form the intellectual base, which are linked to research front articles by forward citations. The underlying intellectual base network is derived from citations made by up to 5000 most-cited research front articles per year during the 15-year period between 2000 and 2014. The first authors of the highest cited references are labeled, notably Takahashi as the first author of the two groundbreaking induced pluripotent stem cells articles.

Figure 3. Among 186 subject categories, 47 subject categories have occurrence bursts during (2000 – 2014).

Figure 4. Keywords with periods of burst from 2009 onward based on up to 5000 most frequently appeared keywords per year for 15 years (2000 – 2014) are shown.

Figure 5. A total of 100 references with the strongest citation bursts over the period between 2000 and 2014 are shown. The burst detection was based on the citations made by the top 5000 articles per year during the 15-year time span.

Table 2. Top five references with the strongest citation bursts during 2000 – 2014.

		Citation burst
Rank	References	Strength	Begin	End	Duration (2000 – 2014)
1	Takahashi and Yamanaka (2006) CELL, V126, P663 [6]	427.6	2009	2011
2	Reya et al. (2001) NATURE, V414, P105 [42]	312.5	2002	2006
3	Jiang et al. (2002) NATURE, V418, P41 [43]	255.7	2002	2007
4	Takahashi et al. (2007) CELL, V131, P861 [35]	226.2	2009	2012
5	Jain (2005) SCIENCE, V307, P58 [44]	203.4	2006	2010

Table 3. References with the most recent bursts from 2011.

		Citation burst
Rank	References (#)	Strength	Begin	End	Duration (2000 – 2014)
1	Warren et al. (2010) CELL STEM CELL, V7, P618 [45]	113.0	2011	2014
2	Kim et al. (2010) NATURE, V467, P285 [32]	102.8	2011	2014
3	Vierbuchen et al. (2010) NATURE, V463, P1035 [23]	93.7	2011	2014
4	Ieda et al. (2010) CELL, V142, P375 [22]	90.7	2011	2014
5	Lister et al. (2011) NATURE, V471, P68 [46]	90.1	2011	2014
6	Gore et al. (2011) NATURE, V471, P63 [17]	73.0	2011	2014
7	Slaughter et al. (2009) ADV MATER, V21, P3307 [47]	69.3	2011	2014
8	Polo et al. (2010) NAT BIOTECHNOL, V28, P848 [48]	65.3	2011	2014
9	Hanahan and Weinberg (2011) CELL, V144, P646 [31]	93.1	2012	2014
10	Zhao et al. (2011) NATURE, V474, P212 [16]	78.9	2012	2014
11	Anokye-Danso et al. (2011) CELL STEM CELL, V8, P376 [33]	78.7	2012	2014
12	Dasha et al. (2011) PROG POLYM SCI, V36, P981 [34]	71.0	2012	2014

Table 4. The four hot articles with citation bursts since 2012. First authors’ names are used in the references. Additional co-authors, if any, are not included.

Rank	References with citation bursts since 2012
9	Hanahan and Weinberg (2011) [31] Hallmarks of Cancer: The Next Generation. CELL, V144, P646. ‘Conceptual progress in the last decade has added two emerging hallmarks of potential generality to this list – reprogramming of energy metabolism and evading immune destruction’.
10	Zhao et al. (2011) [16] Immunogenicity of induced pluripotent stem cells. NATURE, V474, P212. ‘These findings indicate that, in contrast to derivatives of ESCs, abnormal gene expression in some cells differentiated from iPSCs can induce T-cell-dependent immune response in syngeneic recipients. Therefore, the immunogenicity of therapeutically valuable cells derived from patient-specific iPSCs should be evaluated before any clinic application of these autologous cells into the patients’.
11	Anokye-Danso et al. (2011) [33] Highly efficient miRNA-mediated reprogramming of Mouse and human somatic cells to pluripotency. CELL STEM CELL, V8, P376. ‘This miRNA-based reprogramming approach is two orders of magnitude more efficient than standard Oct4/Sox2/Klf4/Myc-mediated methods’.
12	Dash et al. (2011) [34] Chitosan – A versatile semi-synthetic polymer in biomedical applications. PROG POLYM SCI, V36, P981. ‘Chitosan is a polyelectrolyte with reactive functional groups, gel-forming capability, high adsorption capacity and biodegradability. In addition, it is innately biocompatible and non-toxic to living tissues as well as having antibacterial, antifungal and antitumor activity. These features highlight the suitability and extensive applications that chitosan has in medicine. Micro/nanoparticles and hydrogels are widely used in the design of chitosan-based therapeutic systems. The chemical structure and relevant biological properties of chitosan for regenerative medicine have been summarized as well as the methods for the preparation of controlled drug release devices and their applications’.

ESCs: Embryonic stem cells; iPSCs: Induced pluripotent stem cells.

Figure 6. Illustrations of regenerative medicine (2000 – 2014). Left: Landmark nodes (large citation tree rings) and hotspot articles (citation bursts in red rings). Right: New developments (colored in blue) since our 2011 review, for example, #8 cell sheet engineering and #4 biologic scaffold, versus previously identified areas (colored in red).

Table 5. A list of articles that contributed to clusters #4 control or biologic scaffold and #8 cell sheet engineering.

Cluster #	Rank	Coverage (%)	Representative articles	Ref.
4	1	11	Liu et al. (2010) Synthetic hydrogels for controlled stem cell differentiation	[49]
4	2	10	Kim et al. (2010) Biomimetic nanopatterns as enabling tools for analysis and control of live cells	[50]
4	3	10	Pattersona et al. (2010) Biomimetic materials in tissue engineering	[51]
4	4	10	Roacha et al. (2010) Surface strategies for control of neuronal cell adhesion: a review	[52]
4	5	10	Teo et al. (2010) Nanotopography/mechanical induction of stem-cell differentiation	[53]
8	1	39	Elloumi-Hannachi et al. (2010) Cell sheet engineering: A unique nanotechnology for scaffold-free tissue reconstruction with clinical applications in regenerative medicine	[54]
8	2	35	Kelm and Fusseneggar (2010) Scaffold-fee cell delivery for use in regenerative medicine	[55]
8	3	26	Itogaa and Okanoa (2010) The high functionalization of temperature-responsive culture dishes for establishing advanced cell sheet engineering	[56]
8	4	22	Egami et al. (2014) Latest status of the clinical and industrial applications of cell sheet engineering and regenerative engineering	[57]

Figure 7. A timeline visualization for T_{2000 – 2011} is shown.

Figure 8. A timeline visualization for T_{2000 – 2014} is shown. New developments since 2012 are included in the visualization, notably in association with clusters #5, #8, #11 and #13.

Figure 9. A network of 1552 co-cited references representing citation patterns of top 300 articles per year between 2006 and 2014.

Table 6. Largest clusters of co-cited references among the 294 clusters.

Cluster ID	Size	Silhouette	Average year	Label by TF*IDF	Label by log-likelihood ratio	Label by mutual information
0	101	0.939	2005	Precancerous stem cell	Cancer stem cell	Breast
1	77	0.918	2005	Phosphoinositide	Embryonic stem cell	Sox2
2	77	0.876	2007	Cardiac stem cell therapy	Cardiomyocyte	Developmental paradigm
3	77	0.886	2008	Mesentery-derived cell	Induced pluripotent stem cell	Multipotent isl1
4	62	0.805	2010	β-cell	Induced pluripotent stem cell	Switching
5	58	0.897	2009	Genome-wide identification	Pluripotency	Mutant p53 facilitate
6	55	0.974	2011	Receptor-expressing T-cell	Design	Cancer gene therapy
7	51	0.938	2004	LongSAGE profiling	Human embryonic stem cell	Embryoid body homogeneity
8	50	0.901	2007	Bisulfite sequencing	DNA methylation	Promoter DNA methylation
9	49	0.918	2005	Atlantic salmon	Mesenchymal stem cell	Human skin fibroblast
10	46	0.945	2011	Active mechanical perfusion	Extracellular matrix	Infection
11	45	0.978	2006	IL-6-dependent PGE2 secretion	Mesenchymal stem cell	Allogeneic mesenchymal stem cell therapy
12	41	0.968	2010	New kid	Active DNA demethylation	DNA methyltransferase
13	40	0.87	2010	Extended passaging	Induced pluripotent stem cell	Exploiting pluripotency
14	39	0.872	2004	Cell fusion	Cell fusion	Bone marrow-derived cell therapy
15	39	0.972	2011	Kidney transplantation tolerance	Organ transplantation	Acellular cartilage matrix scaffold
17	37	0.993	2005	Osteoblastic niche	Niche	Defect
16	37	0.933	2011	Human cardiosphere	Myocardial cell sheet therapy	Capturing epidermal stemness
18	33	0.961	2010	Leucine-rich repeat-containing G-protein-coupled receptor	Intestinal stem cell	Aldehyde dehydrogenase
19	32	0.965	2011	Mineralized collagen scaffold	Nanofibrous mat	Cardiac myocyte

Table 7. Articles with the strongest citation bursts in cluster #6.

Citation	Burst	Author	Year	Title	Source	Ref.
118	46.34	Stasi et al.	2011	Inducible apoptosis as a safety switch for adoptive cell therapy	NEW ENGL J MED	[58]
70	26.78	Porter et al.	2011	Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia	NEW ENGL J MED	[59]
44	17.27	Tormin et al.	2011	CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization	BLOOD	[60]
40	15.7	Brentjens et al.	2011	Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias	BLOOD	[61]
34	13.93	Savoldo et al.	2011	CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients	J CLIN INVEST	[62]

Table 8. Articles that cite over 20% members of cluster #6.

Coverage (%)	Articles citing cluster #6	Ref.
36	Ruella and Kalos (2014) Adoptive immunotherapy for cancer	[13]
29	Dotti et al. (2014) Design and development of therapies using chimeric antigen receptor-expressing T cells	[63]
20	Jensen and Riddell (2014) Design and implementation of adoptive therapy with chimeric antigen receptor-modified T cells	[64]
20	Turtle et al. (2012) Engineered T cells for anti-cancer therapy	[65]

Table 9. Articles with the strongest citation bursts in cluster #10.

Citation	Burst	Author	Year	Title	Source	Ref.
129	44.42	Burdick and Prestwich	2011	Hyaluronic acid hydrogels for biomedical applications	ADV MATER	[66]
198	42.57	Ott et al.	2008	Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart	NAT MED	[67]
128	39.17	Dvir et al.	2011	Nanotechnological strategies for engineering complex tissues	NAT NANOTECHNOL	[68]
129	38.01	Macchiarini et al.	2008	Clinical transplantation of a tissue-engineered airway	LANCET	[69]
164	37.87	Uygun et al.	2010	Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix	NAT MED	[70]

Table 10. Articles with the strongest citation bursts in cluster #15.

Citation	Burst	Author	Year	Title	Source	Ref.
115	35.44	Lee et al.	2011	Growth factor delivery-based tissue engineering: general approaches and a review of recent developments	J R SOC INTERFACE	[71]
104	33.9	Crapo et al.	2011	An overview of tissue and whole organ decellularization processes	BIOMATERIALS	[72]
193	33.8	Badylak et al.	2009	Extracellular matrix as a biological scaffold material: Structure and function	ACTA BIOMATER	[36]
128	29.44	Chen et al.	2010	Toward delivery of multiple growth factors in tissue engineering	BIOMATERIALS	[73]
76	27.06	Hoppe et al.	2011	A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics	BIOMATERIALS	[74]

Table 11. Articles with the strongest citation bursts in cluster #16.

Citation	Burst	Author	Year	Title	Source	Ref.
164	64.43	Bolli et al.	2011	Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised Phase I trial	LANCET	[37]
177	52.88	Hare et al.	2009	A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction	J AM COLL CARDIOL	[75]
118	46.34	Makkar et al.	2012	Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised Phase I trial	LANCET	[76]
114	44.22	Williams and Hare	2011	Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease	CIRC RES	[77]
119	35.12	Karussis et al.	2010	Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis	ARCH NEUROL-CHICAGO	[78]

Figure 10. An alluvial flow visualization of highly co-cited articles based on a 15-year period (2000 – 2014) is shown. Each year’s network is formed by references made by top 100 citing articles and pruned by Pathfinder Network Scaling. For each node, the five strongest connections are retained. The look-back time is limited up to 5 years.

Figure 11. Alluvial flow of terms is shown. Each year top 100 noun phrases formed a Pathfinder network.

Figure 12. A network of 6130 articles from the combined dataset of 71,393 one-step citation expansion is shown. Articles are grouped based on their bibliographic coupling. The largest four clusters are #0 mesenchymal stem cell, #1 DNA methylation, #2 transforming growth and #3 biomedical application.

Table 12. The largest five clusters in the 6130-article network.

Cluster ID	Size	Silhouette	Mean (year)	Label (TFIDF)	Label (LLR)	Label (MI)
0	180	0.999	2006	Cumulus cell	Mesenchymal stem cell	Depletion
1	158	1	2013	Action mechanism	DNA methylation	Corticofugal neuron
2	149	1	2005	Systemic sclerosis	Transforming growth	Adult hippocampus
3	147	1	2011	Antibiotic	Biomedical application	Direct comparison
4	137	1	2004	Silico	Silico	Gene-expression profiling

LLR: Log-likelihood ratio; MI: Mutual information; TFIDF: Term frequency x inversed document frequency.

Figure 13. A dual-map overlay of dataset D_A, which contains 3875 articles published between 2000 and 2011 is shown.

Figure 14. Dual-map overlays of the most-cited articles published between 2012 and 2014 on top of the D_A overlay are shown. In particular, references made by 2012 articles are shown in green, references made by 2013 articles are shown in orange, and references made by 2014 articles are shown in red.

Figure 15. Stadtfeld and Hochedlinger (2010) bridged three clusters #2, #5 and #12.

Table 13. Articles with the strongest structural variation potential score (weighted cluster linkage) based on structural properties during the period between 2006 and 2011.

Cluster linkage weighted by CR NR	Centrality divergence	Global cites	Title	Reference
2.0045	0.7845	223	Induced pluripotency: history mechanisms and applications [9]	Stadtfeld and Hochedlinger (2010) GENE DEV, V24, P2239
1.4161	0.8324	12	Experimental approaches for the generation of induced pluripotent stem cells [79]	Sommer and Mostoslavsky (2010) STEM CELL RES THER, V1, P26
1.3542	0.8828	131	Progress toward the clinical application of patient-specific pluripotent stem cells [41]	Kiskinis and Eggan (2010) J CLIN INVEST, V120, P51
1.2186	0.2678	21	The therapeutic potential of stem cells [80]	Watt and Driskell (2010) PHILOS T R SOC B, V365, P155
1.0608	0.6138	10	An introduction to induced pluripotent stem cells [81]	Hanley et al. (2010) BRIT J HAEMATOL, V151, P16
1.0499	0.3606	11	Distinguishing between mouse and human pluripotent stem cell regulation: the best laid plans of mice and men [82]	Schnerch et al. (2010) STEM CELLS, V28, P419
0.9224	0.7125	22	The genetics of induced pluripotency [83]	Ralston and Rossant (2010) REPRODUCTION, V139, P35
0.8444	0.8619	10	Roadblocks en route to the clinical application of induced pluripotent stem cells [84]	Lowry and Quan (2010) J CELL SCI, V123, P643
0.8089	0.2216	11	Molecular characterization of the human NANOG protein [85]	Chang et al. (2009) STEM CELLS, V27, P812
0.7945	0.2826	12	Cell reprogramming: expectations and challenges for chemistry in stem cell biology and regenerative medicine [86]	Anastasia et al. (2010) CELL DEATH DIFFER, V17, P1230

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