AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Article Link
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

Graphene foam/hydrogel scaffolds for regeneration of peripheral nerve using ADSCs in a diabetic mouse model

Qun Huang1,§Yuting Cai2,4,§Xinrui Yang1,3,§Weimin Li1,3,§Hongji Pu1Zhenjing Liu4Hongwei Liu4Mohsen Tamtaji4Feng Xu5Liyuan Sheng6Tae-Hyung Kim7Shiqing Zhao8Dazhi Sun2( )Jinbao Qin1,3( )Zhengtang Luo4( )Xinwu Lu1,3( )
Department of Vascular Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, China
Guangdong Provincial Key Laboratory of Functional Oxide Materials and Devices, Department of Materials Science and Engineering, Southern University of Science and Technology, Shenzhen 518055, China
Vascular Center of Shanghai Jiao Tong University, Shanghai 200011, China
Department of Chemical and Biological Engineering, and William Mong Institute of Nano Science and Technology, the Hong Kong University of Science and Technology, Hong Kong 999077, China
Bioinspired Engineering and Biomechanics Center (BEBC), the Key Laboratory of Biomedical Information Engineering of Ministry of Education, School of Life Science and Technology, Xi'an Jiaotong University, Xi'an 710049, China
Shenzhen Institute, Peking University, Shenzhen 518057, China
School of Integrative Engineering, Chung-Ang University, Seoul 06974, Republic of Korea
School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai 200030, China

§ Qun Huang, Yuting Cai, Xinrui Yang, and Weimin Li contributed equally to this work.

Show Author Information

Graphical Abstract

Adipose-derived stem cells (ADSCs)-loaded graphene foam/hydrogel scaffold promotes the recovery of diabetic peripheral nerve injury.

Abstract

The functional recovery of peripheral nerve injury (PNI) is unsatisfactory, whereas diabetes mellitus (DM) and its related complications further attenuate the restoration of diabetic PNI (DPNI). Adipose-derived stem cells (ADSCs) are promising candidates for treatment of DPNI due to their abundant source, excellent differentiation and paracrine ability. Our results showed that ADSCs remarkably enhanced the proliferation and migration of Schwann cells and endothelial cells, and tube formation. Mechanistically, ADSCs could regulate Nrf2/HO-1, NF-κB and PI3K/AKT/mTOR signaling pathways, showing multiple functions in reducing oxidative stress and inflammation, and regulating cell metabolism, growth, survival, proliferation, angiogenesis, differentiation of Schwann cell and myelin formation. In current study, novel graphene foam (GF)/hydrogel-based scaffold was developed to deliver ADSCs for treatment of DPNI. GF/hydrogel scaffold exhibited excellent mechanical strength, suitable porous network, superior electrical conductivity, and good biocompatibility. In vitro results revealed that GF/hydrogel scaffold could obviously accelerate proliferation of Schwann cells. Moreover, in vivo experiments demonstrated that ADSCs-loaded GF/hydrogel scaffold significantly promoted the recovery of DPNI and inhibited the atrophy of targeted muscles, thus providing a novel and attractive therapeutic approach for DPNI patients.

Electronic Supplementary Material

Download File(s)
12274_2021_3961_MOESM1_ESM.pdf (1.1 MB)

References

1

Faroni, A.; Mobasseri, S. A.; Kingham, P. J.; Reid, A. J. Peripheral nerve regeneration: Experimental strategies and future perspectives. Adv. Drug Deliv. Rev. 2015, 82–83, 160–167.

2

Huang, Q.; Cai, Y. T.; Zhang, X.; Liu, J. C.; Liu, Z. J.; Li, B.; Wong, H.; Xu, F.; Sheng, L. Y.; Sun, D. Z. et al. Aligned graphene mesh-supported double network natural hydrogel conduit loaded with netrin-1 for peripheral nerve regeneration. ACS Appl. Mater. Interfaces 2021, 13, 112–122.

3

Li, R.; Li, Y. Y.; Wu, Y. Q.; Zhao, Y. Z.; Chen, H. W.; Yuan, Y.; Xu, K.; Zhang, H. Y.; Lu, Y. F.; Wang, J. et al. Heparin-poloxamer thermosensitive hydrogel loaded with bFGF and NGF enhances peripheral nerve regeneration in diabetic rats. Biomaterials 2018, 168, 24–37.

4

Zimmet, P.; Alberti, K. G.; Magliano, D. J.; Bennett, P. H. Diabetes mellitus statistics on prevalence and mortality: Facts and fallacies. Nat. Rev. Endocrinol. 2016, 12, 616–622.

5

Singh, B.; Singh, V.; Krishnan, A.; Koshy, K.; Martinez, J. A.; Cheng, C.; Almquist, C.; Zochodne, D. W. Regeneration of diabetic axons is enhanced by selective knockdown of the PTEN gene. Brain 2014, 137, 1051–1067.

6

Vijayavenkataraman, S. Nerve guide conduits for peripheral nerve injury repair: A review on design, materials and fabrication methods. Acta Biomater. 2020, 106, 54–69.

7

Carriel, V.; Garrido-Gómez, J.; Hernández-Cortés, P.; Garzón, I.; García-García, S.; Sáez-Moreno, J. A.; Del Carmen Sánchez-Quevedo, M.; Campos, A.; Alaminos, M. Combination of fibrin-agarose hydrogels and adipose-derived mesenchymal stem cells for peripheral nerve regeneration. J. Neural Eng. 2013, 10, 026022.

8

Kershaw, E. E.; Flier, J. S. Adipose tissue as an endocrine organ. J. Clin. Endocrinol. Metab. 2004, 89, 2548–2556.

9

Kern, P. A.; Ranganathan, S.; Li, C. L.; Wood, L.; Ranganathan, G. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am. J. Physiol. :Endocrinol. Metab. 2001, 280, E745–E751.

10

Yudkin, J. S.; Kumari, M.; Humphries, S. E.; Mohamed-Ali, V. Inflammation, obesity, stress and coronary heart disease: Is interleukin-6 the link? Atherosclerosis 2000, 148, 209–214.

11

Rigotti, G.; Marchi, A.; Galiè, M.; Baroni, G.; Benati, D.; Krampera, M.; Pasini, A.; Sbarbati, A. Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant: A healing process mediated by adipose-derived adult stem cells. Plast. Reconstr. Surg. 2007, 119, 1409–1422.

12

Bacakova, L.; Zarubova, J.; Travnickova, M.; Musilkova, J.; Pajorova, J.; Slepicka, P.; Kasalkova, N. S.; Svorcik, V.; Kolska, Z.; Motarjemi, H. et al. Stem cells: Their source, potency and use in regenerative therapies with focus on adipose-derived stem cells— A review. Biotechnol. Adv. 2018, 36, 1111–1126.

13

Mu, Y.; Wu, F.; Lu, Y. R.; Wei, L. M.; Yuan, W. E. Progress of electrospun fibers as nerve conduits for neural tissue repair. Nanomedicine 2014, 9, 1869–1883.

14

Quigley, A. F.; Bulluss, K. J.; Kyratzis, I. L. B.; Gilmore, K.; Mysore, T.; Schirmer, K. S. U.; Kennedy, E. L.; O'Shea, M.; Truong, Y. B.; Edwards, S. L. et al. Engineering a multimodal nerve conduit for repair of injured peripheral nerve. J. Neural Eng. 2013, 10, 016008.

15

Kusuhara, H.; Hirase, Y.; Isogai, N.; Sueyoshi, Y. A clinical multi-center registry study on digital nerve repair using a biodegradable nerve conduit of PGA with external and internal collagen scaffolding. Microsurgery 2019, 39, 395–399.

16

Singh, S.; Srivastava, A. K.; Baranwal, A. K.; Bhatnagar, A.; Das, K. K.; Jaiswal, S.; Behari, S. Efficacy of silicone conduit in the rat sciatic nerve repair model: Journey of a thousand miles. Neurol. India 2021, 69, 318.

17

Bryan, D. J.; Tang, J. B.; Doherty, S. A.; Hile, D. D.; Trantolo, D. J.; Wise, D. L.; Summerhayes, I. C. Enhanced peripheral nerve regeneration through a poled bioresorbable poly (lactic-co-glycolic acid) guidance channel. J. Neural Eng. 2004, 1, 91–98.

18

Burnstine-Townley, A.; Eshel, Y.; Amdursky, N. Conductive scaffolds for cardiac and neuronal tissue engineering: Governing factors and mechanisms. Adv. Funct. Mater. 2020, 30, 1901369.

19

Sun, J. Y.; Zhao, X. H.; Illeperuma, W. R. K.; Chaudhuri, O.; Oh, K. H.; Mooney, D. J.; Vlassak, J. J.; Suo, Z. G. Highly stretchable and tough hydrogels. Nature 2012, 489, 133–136.

20

Haque, M. A.; Kurokawa, T.; Gong, J. P. Super tough double network hydrogels and their application as biomaterials. Polymer 2012, 53, 1805–1822.

21

Qian, Y.; Song, J. L.; Zhao, X. T.; Chen, W.; Ouyang, Y. M.; Yuan, W. E.; Fan, C. Y. 3D fabrication with integration molding of a graphene oxide/polycaprolactone nanoscaffold for neurite regeneration and angiogenesis. Adv. Sci. 2018, 5, 1700499.

22

Yuan, H. H.; Qin, J. B.; Xie, J.; Li, B. Y.; Yu, Z. P.; Peng, Z. Y.; Yi, B. C.; Lou, X. X.; Lu, X. W.; Zhang, Y. Z. Highly aligned core−shell structured nanofibers for promoting phenotypic expression of vSMCs for vascular regeneration. Nanoscale 2016, 8, 16307–16322.

23

Imaninezhad, M.; Pemberton, K.; Xu, F. L.; Kalinowski, K.; Bera, R.; Zustiak, S. P. Directed and enhanced neurite outgrowth following exogenous electrical stimulation on carbon nanotube-hydrogel composites. J. Neural Eng. 2018, 15, 056034.

24

Niu, Y. M.; Chen, X. F.; Yao, D. Y.; Peng, G.; Liu, H. F.; Fan, Y. B. Enhancing neural differentiation of induced pluripotent stem cells by conductive graphene/silk fibroin films. J. Biomed. Mater. Res. 2018, 106, 2973–2983.

25

Baranes, K.; Shevach, M.; Shefi, O.; Dvir, T. Gold nanoparticle-decorated scaffolds promote neuronal differentiation and maturation. Nano Lett. 2016, 16, 2916–2920.

26

Xu, H. X.; Holzwarth, J. M.; Yan, Y. H.; Xu, P. H.; Zheng, H.; Yin, Y. X.; Li, S. P.; Ma, P. X. Conductive PPY/PDLLA conduit for peripheral nerve regeneration. Biomaterials 2014, 35, 225–235.

27

Abidi, I. H.; Liu, Y. Y.; Pan, J.; Tyagi, A.; Zhuang, M. H.; Zhang, Q. C.; Cagang, A. A.; Weng, L. T.; Sheng, P.; Goddard III, W. A. et al. Regulating top-surface multilayer/single-crystal graphene growth by “gettering” carbon diffusion at backside of the copper foil. Adv. Funct. Mater. 2017, 27, 1700121.

28

Chen, Z. P.; Ren, W. C.; Gao, L. B.; Liu, B. L.; Pei, S. F.; Cheng, H. M. Three-dimensional flexible and conductive interconnected graphene networks grown by chemical vapour deposition. Nat. Mater. 2011, 10, 424–428.

29

Novoselov, K. S.; Geim, A. K.; Morozov, S. V.; Jiang, D.; Zhang, Y.; Dubonos, S. V.; Grigorieva, I. V.; Firsov, A. A. Electric field effect in atomically thin carbon films. Science 2004, 306, 666–669.

30

Dikin, D. A.; Stankovich, S.; Zimney, E. J.; Piner, R. D.; Dommett, G. H. B.; Evmenenko, G.; Nguyen, S. T.; Ruoff, R. S. Preparation and characterization of graphene oxide paper. Nature 2007, 448, 457–460.

31

Song, Q.; Jiang, Z. Y.; Li, N.; Liu, P.; Liu, L. W.; Tang, M. L.; Cheng, G. S. Anti-inflammatory effects of three-dimensional graphene foams cultured with microglial cells. Biomaterials 2014, 35, 6930–6940.

32

Bahremandi Tolou, N.; Salimijazi, H.; Kharaziha, M.; Faggio, G.; Chierchia, R.; Lisi, N. A three-dimensional nerve guide conduit based on graphene foam/polycaprolactone. Mater. Sci. Eng. :C 2021, 126, 112110.

33

Guo, R. R.; Li, J.; Chen, C. T.; Xiao, M.; Liao, M. H.; Hu, Y. N.; Liu, Y.; Li, D.; Zou, J.; Sun, D. P. et al. Biomimetic 3D bacterial cellulose-graphene foam hybrid scaffold regulates neural stem cell proliferation and differentiation. Colloids Surf. B:Biointerfaces 2021, 200, 111590.

34

Fang, Q. J.; Zhang, Y. H.; Chen, X. B.; Li, H.; Cheng, L. Y.; Zhu, W. J.; Zhang, Z.; Tang, M. L.; Liu, W.; Wang, H. et al. Three-dimensional graphene enhances neural stem cell proliferation through metabolic regulation. Front. Bioeng. Biotechnol. 2019, 7, 436.

35

Li, N.; Zhang, Q.; Gao, S.; Song, Q.; Huang, R.; Wang, L.; Liu, L. W.; Dai, J. W.; Tang, M. L.; Cheng, G. S. Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells. Sci. Rep. 2013, 3, 1604.

36

Tasnim, N.; Thakur, V.; Chattopadhyay, M.; Joddar, B. The efficacy of graphene foams for culturing mesenchymal stem cells and their differentiation into dopaminergic neurons. Stem Cells Int. 2018, 2018, 3410168.

37

Li, Z. H.; Wang, H. Q.; Yang, B.; Sun, Y. K.; Huo, R. Three-dimensional graphene foams loaded with bone marrow derived mesenchymal stem cells promote skin wound healing with reduced scarring. Mater. Sci. Eng. :C 2015, 57, 181–188.

38

Li, J.; Celiz, A. D.; Yang, J.; Yang, Q.; Wamala, I.; Whyte, W.; Seo, B. R.; Vasilyev, N. V.; Vlassak, J. J.; Suo, Z. et al. Tough adhesives for diverse wet surfaces. Science 2017, 357, 378–381.

39

Cai, Y. T.; Qin, J. B.; Li, W. M.; Tyagi, A.; Liu, Z. J.; Hossain, M. D.; Chen, H. M.; Kim, J. K.; Liu, H. W.; Zhuang, M. H. et al. A stretchable, conformable, and biocompatible graphene strain sensor based on a structured hydrogel for clinical application. J. Mater. Chem. A 2019, 7, 27099–27109.

40

Qin, J. B.; Li, K. A.; Li, X. X.; Xie, Q. S.; Lin, J. Y.; Ye, K. C.; Jiang, M. E.; Zhang, G. X.; Lu, X. W. Long-term MRI tracking of dual-labeled adipose-derived stem cells homing into mouse carotid artery injury. Int. J. Nanomed. 2012, 7, 5191–5203.

41

Harley, B. A.; Hastings, A. Z.; Yannas, I. V.; Sannino, A. Fabricating tubular scaffolds with a radial pore size gradient by a spinning technique. Biomaterials 2006, 27, 866–874.

42

Losurdo, M.; Giangregorio, M. M.; Capezzuto, P.; Bruno, G. Graphene CVD growth on copper and nickel: Role of hydrogen in kinetics and structure. Phys. Chem. Chem. 2011, 13, 20836–20843.

43

Wirth, C.; Grosgogeat, B.; Lagneau, C.; Jaffrezic-Renault, N.; Ponsonnet, L. Biomaterial surface properties modulate in vitro rat calvaria osteoblasts response: Roughness and or chemistry? Mater. Sci. Eng. :C 2008, 28, 990–1001.

44

Lv, Z. Y.; Li, X. L.; Chen, Z. H.; Chen, J.; Chen, C.; Xiong, P.; Sun, T. L.; Qing, G. Y. Surface stiffness-a parameter for sensing the chirality of saccharides. ACS Appl. Mater. Interfaces 2015, 7, 27223–27233.

45

Nectow, A. R.; Marra, K. G.; Kaplan, D. L. Biomaterials for the development of peripheral nerve guidance conduits. Tissue Eng. Part B:Rev. 2012, 18, 40–50.

46

Borschel, G. H.; Kia, K. F.; Kuzon, W. M. Jr.; Dennis, R. G. Mechanical properties of acellular peripheral nerve. J. Surg. Res. 2003, 114, 133–139.

47

Qian, Y.; Zhao, X. T.; Han, Q. X.; Chen, W.; Li, H.; Yuan, W. E. An integrated multi-layer 3D-fabrication of PDA/RGD coated graphene loaded PCL nanoscaffold for peripheral nerve restoration. Nat. Commun. 2018, 9, 323.

48

Golafshan, N.; Kharaziha, M.; Fathi, M. Tough and conductive hybrid graphene-PVA: Alginate fibrous scaffolds for engineering neural construct. Carbon 2017, 111, 752–763.

49

Wang, J.; Cheng, Y.; Chen, L.; Zhu, T. H.; Ye, K. Q.; Jia, C.; Wang, H. J.; Zhu, M. F.; Fan, C. Y.; Mo, X. M. In vitro and in vivo studies of electroactive reduced graphene oxide-modified nanofiber scaffolds for peripheral nerve regeneration. Acta Biomater. 2019, 84, 98–113.

50

Chung, M. T.; Zimmermann, A. S.; Paik, K. J.; Morrison, S. D.; Hyun, J. S.; Lo, D. D.; McArdle, A.; Montoro, D. T.; Walmsley, G. G.; Senarath-Yapa, K. et al. Isolation of human adipose-derived stromal cells using laser-assisted liposuction and their therapeutic potential in regenerative medicine. Stem Cells Transl. Med. 2013, 2, 808–817.

51

Huang, Q. T.; Zou, Y. J.; Arno, M. C.; Chen, S.; Wang, T.; Gao, J. Y.; Dove, A. P.; Du, J. Z. Hydrogel scaffolds for differentiation of adipose-derived stem cells. Chem. Soc. Rev. 2017, 46, 6255–6275.

52

Jiang, L. F.; Jones, S.; Jia, X. F. Stem cell transplantation for peripheral nerve regeneration: Current options and opportunities. Int. J. Mol. Sci. 2017, 18, 94.

53

Qian, Y.; Han, Q. X.; Zhao, X. T.; Song, J. L.; Cheng, Y.; Fang, Z. W.; Ouyang, Y. M.; Yuan, W. E.; Fan, C. Y. 3D melatonin nerve scaffold reduces oxidative stress and inflammation and increases autophagy in peripheral nerve regeneration. J. Pineal Res. 2018, 65, e12516.

54

Paneni, F.; Costantino, S.; Castello, L.; Battista, R.; Capretti, G.; Chiandotto, S.; D'Amario, D.; Scavone, G.; Villano, A.; Rustighi, A. et al. Targeting prolyl-isomerase Pin1 prevents mitochondrial oxidative stress and vascular dysfunction: Insights in patients with diabetes. Eur. Heart J. 2015, 36, 817–828.

55

Chen, X. X.; Ren, X. X.; Zhang, L. L.; Liu, Z. J.; Hai, Z. J. Mitochondria-targeted fluorescent and photoacoustic imaging of hydrogen peroxide in inflammation. Anal. Chem. 2020, 92, 14244–14250.

56

Hervera, A.; De Virgiliis, F.; Palmisano, I.; Zhou, L. M.; Tantardini, E.; Kong, G. P.; Hutson, T.; Danzi, M. C.; Perry, R. B. T.; Santos, C. X. C. et al. Reactive oxygen species regulate axonal regeneration through the release of exosomal NADPH oxidase 2 complexes into injured axons. Nat. Cell Biol. 2018, 20, 307–319.

57

Akhavan, O. Graphene scaffolds in progressive nanotechnology/stem cell-based tissue engineering of the nervous system. J. Mater. Chem. B 2016, 4, 3169–3190.

58

Mizunoe, Y.; Kobayashi, M.; Sudo, Y.; Watanabe, S.; Yasukawa, H.; Natori, D.; Hoshino, A.; Negishi, A.; Okita, N.; Komatsu, M. et al. Trehalose protects against oxidative stress by regulating the Keap1-Nrf2 and autophagy pathways. Redox Biol. 2018, 15, 115–124.

59

Hayden, M. S.; Ghosh, S. Shared principles in NF-κB signaling. Cell 2008, 132, 344–362.

60

Ediriweera, M. K.; Tennekoon, K. H.; Samarakoon, S. R. Role of the PI3K/AKT/mTOR signaling pathway in ovarian cancer: Biological and therapeutic significance. Semin. Cancer Biol. 2019, 59, 147–160.

61

Ishii, A.; Furusho, M.; Bansal, R. Mek/ERK1/2-MAPK and PI3K/Akt/mtor signaling plays both independent and cooperative roles in schwann cell differentiation, myelination and dysmyelination. GLIA 2021, 69, 2429–2446.

62

Askari, M.; Naniz, M. A.; Kouhi, M.; Saberi, A.; Zolfagharian, A.; Bodaghi, M. Recent progress in extrusion 3D bioprinting of hydrogel biomaterials for tissue regeneration: A comprehensive review with focus on advanced fabrication techniques. Biomater. Sci. 2021, 9, 535–573.

63

Slaughter, B. V.; Khurshid, S. S.; Fisher, O. Z.; Khademhosseini, A.; Peppas, N. A. Hydrogels in regenerative medicine. Adv. Mater. 2009, 21, 3307–3329.

64

Zhang, K. H.; Zheng, H. H.; Liang, S.; Gao, C. Y. Aligned PLLA nanofibrous scaffolds coated with graphene oxide for promoting neural cell growth. Acta Biomater. 2016, 37, 131–142.

65

Cellot, G.; Cilia, E.; Cipollone, S.; Rancic, V.; Sucapane, A.; Giordani, S.; Gambazzi, L.; Markram, H.; Grandolfo, M.; Scaini, D. et al. Carbon nanotubes might improve neuronal performance by favouring electrical shortcuts. Nat. Nanotechnol. 2009, 4, 126–133.

66

Stratton, J. A.; Holmes, A.; Rosin, N. L.; Sinha, S.; Vohra, M.; Burma, N. E.; Trang, T.; Midha, R.; Biernaskie, J. Macrophages regulate schwann cell maturation after nerve injury. Cell Rep. 2018, 24, 2561–2572.e6.

67

Eming, S. A.; Martin, P.; Tomic-Canic, M. Wound repair and regeneration: Mechanisms, signaling, and translation. Sci. Transl. Med. 2014, 6, 265sr6.

68

Morland, C.; Andersson, K. A.; Haugen, Ø. P.; Hadzic, A.; Kleppa, L.; Gille, A.; Rinholm, J. E.; Palibrk, V.; Diget, E. H.; Kennedy, L. H. et al. Exercise induces cerebral VEGF and angiogenesis via the lactate receptor HCAR1. Nat. Commun. 2017, 8, 15557.

69

Kurapati, R.; Mukherjee, S. P.; Martín, C.; Bepete, G.; Vázquez, E.; Pénicaud, A.; Fadeel, B.; Bianco, A. Degradation of single-layer and few-layer graphene by neutrophil myeloperoxidase. Angew. Chem., Int. Ed. 2018, 57, 11722–11727.

70

Yang, K.; Zhang, S.; Zhang, G. X.; Sun, X. M.; Lee, S. T.; Liu, Z. Graphene in mice: Ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Lett. 2010, 10, 3318–3323.

Nano Research
Pages 3434-3445
Cite this article:
Huang Q, Cai Y, Yang X, et al. Graphene foam/hydrogel scaffolds for regeneration of peripheral nerve using ADSCs in a diabetic mouse model. Nano Research, 2022, 15(4): 3434-3445. https://doi.org/10.1007/s12274-021-3961-3
Topics:

1015

Views

12

Crossref

12

Web of Science

10

Scopus

1

CSCD

Altmetrics

Received: 25 July 2021
Revised: 26 October 2021
Accepted: 29 October 2021
Published: 15 December 2021
© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2021
Return