Skip to main content
PMC home page
Heliyon logoLink to Heliyon
. 2024 Sep 5;10(18):e37492. doi: 10.1016/j.heliyon.2024.e37492

Bibliometric analysis of skeletal muscle ischemia/reperfusion (I/R) research from 1986 to 2022

Ming Zhou 1,1, Xueyuan Jia 1,1, Hao Liu 1,1, Yuan Xue 1, Yapeng Wang 1, Zeqing Li 1, Yongwei Wu 1,⁎⁎, Yongjun Rui 1,⁎
PMCID: PMC11416534  PMID: 39309867

Abstract

Introduction

Tissue damage due to ischemia and reperfusion is a critical medical problem worldwide. Studies in this field have made remarkable advances in understanding the pathogenesis of ischemia/reperfusion (I/R) injury and its treatment with new and known drugs. However, no bibliometric analysis exists in this area of research.

Methods

Research articles and reviews related to skeletal muscle I/R from 1986 to 2022 were retrieved from the Web of Science Core Collection. Bibliometric analysis was performed using Microsoft Excel 2019, VOSviewer (version 1.6.19), Bibliometrix (R-Tool for R-Studio), and CiteSpace (version 6.1.R5).

Results

A total of 3682 research articles and reviews from 2846 institutions in 83 countries were considered in this study. Most studies were conducted in the USA. Hobson RW (UMDNJ-New Jersey Medical School) had the highest publication, and Korthuis RJ (Louisiana State University) had the highest co-citations. Our analysis showed that, though the Journal of Surgical Research was most favored, the Journal of Biological Chemistry had the highest number of co-citations. The pathophysiology, interventions, and molecular mechanisms of skeletal muscle I/R injury emerged as the primary research areas, with “apoptosis,” “signaling pathway,” and “oxidative stress” as the main keywords of research hotspots.

Conclusions

This study provides a thorough overview of research trends and focal points in skeletal muscle I/R injury by applying bibliometric and visualization techniques. The insights gained from our findings offer a profound understanding of the evolving landscape of skeletal muscle I/R injury research, thereby functioning as a valuable reference and roadmap for future investigations.

Keywords: CiteSpace, VOSviewer, Bibliometric, Skeletal muscle ischemia/reperfusion injury, Visual analysis

1. Introduction

Ischemia/reperfusion (I/R) injury is the functional and structural changes that occur in the tissue during the restoration of the blood flow after a period of ischemia. Restoring blood flow often results in harmful effects such as necrosis of irreversibly damaged cells, marked cell swelling, and non-uniform blood flow to the tissue, leading to the deterioration of organ function [1]. This type of injury is often secondary to hemodialysis after severe limb ischemia, bone and soft tissue injury, vascular injury, osteofascial compartment syndrome, hemorrhagic or traumatic shock, and prolonged tourniquet use [[2], [3], [4]]. Skeletal muscles have high metabolic activity and are prone to ischemia-reperfusion injury [5]. Even with rapid restoration of blood flow after severe ischemia, I/R injury can lead to permanent skeletal muscle damage and necrosis or even amputation and multi-organ failure. Since its discovery [2,6], I/R has been studied extensively. Most literature provides a basic understanding of the pathophysiology of I/R injury and many prevention and treatment methods [4,7,8], some of which have successfully protected against the deleterious effects of I/R [9,10]. A systematic analysis of the scientific results and the current status of the field from a global perspective [6] will further help reveal future trends and hot spots of skeletal muscle I/R injury research.

A Bibliometric analysis helps to understand trends and frontiers in various research areas through qualitative and quantitative analysis of relevant scientific publications [11]. It compares scientific output and the impact of different countries, institutions, journals, and scholars [12] on salient research topics and provides valuable references and/or guidance for further scientific research. In recent years, bibliometric studies have been conducted on prime research topics such as stroke [13], autoimmune diseases [14], pulmonary arterial hypertension [15], periodontology [16], orthopedics [17], plastic [18], nursing [19], and other medical fields using software such as CiteSpace, VOSviewer, and the R package “bibliometrix” [20,21]. However, a bibliometric study on skeletal muscle I/R injury commonly encountered in surgical practice is lacking. This extensive analysis of the literature on skeletal muscle ischemia-reperfusion injury uses a bibliometric strategy to assess the current status and hot spots in I/R injury research and predict future research directions.

2. Materials and methods

2.1. Data sources and search strategies

Research articles and reviews on ischemia-reperfusion injury were collected from the Web of Science Core Collection (WoSCC) database of Clarivate, one of the most authoritative and comprehensive database platforms, containing more than 12,000 international academic journals [22,23]. Therefore, we chose it to access global scholarly information for bibliometric analysis [24]. The literature search was performed from the date of creation to March 16, 2023, using the search terms: ((TS=(Reperfusion) OR TS=(Reperfusion Injury)) AND ((TS=(muscle, skeletal)) OR TS=(Hindlimb))) AND (LA= (“ENGLISH”) AND DT=(“ARTICLE” OR “REVIEW")).

Inclusion criteria: (1) articles and reviews in the English language; (2) keywords related to reperfusion and its associated injuries in the context of skeletal muscle and hindlimb.

Exclusion criteria: (1) proceedings papers, which were not considered appropriate for the study's scope; (2) meeting abstracts, which typically lack the depth required for a thorough analysis; (3) book chapters, as they often present a broader overview rather than focused research findings; (4) editorial material, early access publications, notes, letters, and corrections, which do not contribute to the empirical body of knowledge; (5) retracted and non-English publications.

All valid data of the literature, including the year of publication, title, author's name, nationality, affiliation, abstract, keywords, and journal name, were saved in download.txt file format (refer to Appendix 1) from the WoSCC database and imported into Excel 2019 on the same day (March 16, 2023), to mitigate any potential bias arising from frequent database updates. The co-authors (Ming Zhou and Xueyuan Jia) independently searched and extracted all information from these documents. Any disagreement was resolved by consultation with experts to reach a final consensus. Finally, all co-authors used Excel 2019 to clean and analyze the data.

2.2. Data analysis

Visual analysis was performed using Microsoft Excel 2019, VOSviewer (version 1.6.19), Bibliometrix (R-Tool for R-Studio), and CiteSpace (version 6.1.R5). VOSviewer is a bibliometric analysis software that can extract vital information from numerous publications and is commonly used to build collaborative, co-citation, and co-occurrence networks [25]. We used the VOSviewer for country and institution analysis, journal and co-cited journal, author and co-cited author, and keyword co-occurrence analysis. In the VOSviewer map, a node represents an element such as country, institution, journal, and author. The size and color of the nodes indicate the number and classification of these items. The line thickness between two nodes reflects the level of collaboration or co-citation. CiteSpace, a bibliometric analysis and visualization software developed by Professor Chen [26,27], was used for dual-map overlay of journals, keyword, timeline, and citation burst analysis. The R package “bibliometrix” (https://www. bibliometrix.org) was used for thematic evolution analysis and to construct a global distribution network and three-field plot analysis of skeletal muscle ischemia-reperfusion injury publications [28]. For VOSviewer, the parameters were set as follows: Method (Linlog/modularity), with minimum document counts of 3 for a Country/region, 5 for an institution, 3 for an author, 30 for a co-cited author, 20 for a journal, 100 for co-cited journals, 30 for co-cited references, and 20 for keywords. For CiteSpace, the parameters were configured as follows: a time span from 1986 to 2023, with one year per slice and a selection criterion of the Top 50. The remaining parameters were set to default values. For bibliometrix, the “Source by Bradford Law Zones” was selected as “All Sources”. In the three-field plot, the number of items for authors, keywords, and journals were set to 10, 9, and 8, respectively. The other parameters were set to default values.

Journal Citations Reports (JCR) quartile and impact factor (IF) were obtained from Citation Reports 2023. The Hirsch index (H-index, https://www.scimagojr.com) was used to measure the impact and productivity of scientific research [29]. The 2022 gross domestic product (GDP) data for different countries has been sourced from the official website of the World Bank, which can be accessed at https://data.worldbank.org.cn. Quantitative analysis and visual graphs of publications were performed using Microsoft Office Excel 2019.

Acknowledging the potential ambiguity among Chinese authors with similar names, such as Zhang Shan and Zhang Song, we implemented a meticulous disambiguation process to ensure accurate authorship analysis. We cross-checked full names, including middle names or second initials, and utilized institutional affiliations to distinguish authors. In cases where these methods were insufficient, we manually verified authorship using original articles, acknowledgments, or contact details, thus ensuring correct identification and attribution of each author's works.

No ethical review was required since all raw data used here were obtained from public databases.

2.3. Statistical analysis

We compared the Impact Factor (2022), JCR quartile (2022), and H-index (2022) of the top 20 journals in terms of the number of articles with the top 20 co-cited journals using t-test (parametric continuous variable) and Mann-Whitney U (categorical variable). Statistical analysis was performed with SPSS 26.0 (IBM, Armonk, NY, USA), and the significance was set at 2-tailed p < 0.05.

3. Results

3.1. Quantitative analysis of publication

A literature search on March 16, 2023, yielded 3922 documents. After excluding proceeding papers (n = 226), meeting abstracts (n = 147), book chapters (n = 32), editorial material (n = 26), early access (n = 13), notes (n = 9), letter (n = 8), correction (n = 4), the retracted publications (n = 4), corrections, additions (n = 1), and 45 non-English publications, a total of 3682 works of literature were included in the study (Fig. 1).

Fig. 1.

Fig. 1

Open in a new tab

Flow chart of scientometric analysis.

We observed a steady annual growth trend in the global volume of literature published on ischemia-reperfusion injury (Fig. 2). The number of documents increased annually from 1 (1986) to 161 (2018). Most studies were published in 2021 (161, 4.37 %). The year 2000 showed a clear demarcation point. From 1986 to 1999, this field was developed, with 824 papers published in 14 years. From 2000 to 2013, there was a qualitative leap, with 1,622 articles published in 14 years, almost twice as many as in the previous period. These results show that skeletal muscle ischemia-reperfusion injury is a hot research topic.

Fig. 2.

Fig. 2

Open in a new tab

Annual publications between 1986 and 2023. The data for 2023 is not complete.

3.2. Country/region and institutional analysis

Eighty-three countries or regions have published studies on skeletal muscle I/R injury. The bulk of publications came from countries mainly in the northern hemisphere. Only eight countries (10.8 %) from the southern hemisphere, namely Australia, Brazil, New Zealand, Chile, South Africa, Argentina, Peru, and Uruguay (Fig. 3A), contributed to the I/R injury literature. The top ten countries in terms of the number of papers published are shown in Table 1. The United States of America was the most significant contributor, with more than one-third of the total publications (1334, 36.2 %). It was followed by China (327 papers, 8.9 %), Canada (265 papers, 7.2 %), and Germany (249 papers, 6.7 %). A collaborative network was constructed with 74 countries having annual publications ≥3, based on the number of publications and relationships between countries or regions (Fig. 3B). We observed that links between countries were concentrated in the northern hemisphere. The United States of America showed strong collaborations with European countries, while China showed relatively fewer collaborations with other countries.

Fig. 3.

Fig. 3

Open in a new tab

Visualization analysis of country/regions. (A) The network visualization of geographical distribution. (B) Collaboration analysis of countries/regions. Node size is proportional to the number of publications by country/region, and the line thickness between nodes indicates the intensity of co-operation between countries/regions.

Table 1.

Top 10 country/region on research of skeletal muscle ischemia-reperfusion injury.

Rank Country/Region Number of Publication % of Total Publication H-index GDP ($, trillion) Continents
1 USA 1334 36.23 2711 23.32 North America
2 China 327 8.88 1112 17.73 Asia
3 Canada 265 7.2 1381 1.99 North America
4 Germany 249 6.76 1498 4.26 Europe
5 Japan 213 5.78 1171 4.94 Asia
6 England 196 5.32 1707 3.13 Europe
7 Turkey 193 5.24 535 0.82 Asia
8 Italy 145 3.94 1189 2.11 Europe
9 France 122 3.31 1352 2.96 Europe
10 Australia 92 2.5 1193 1.55 Oceania
Open in a new tab

Our study showed that 2846 institutions are involved in skeletal muscle I/R injury research, with seven out of the top ten institutions in the USA (Table 2). The four institutions with the most publications were Harvard University (n = 118, 3.2 %), University of Toronto (n = 58, 1.6 %), University of California San Diego (n = 51, 1.4 %), and University of Western Ontario (n = 41, 1.1 %). The collaborative network based on the number of publications and relationships between institutions having at least five annual publications (Fig. 4) showed that Harvard University, Brigham and Women's Hospital, Boston University, and Massachusetts General Hospital collaborated very closely.

Table 2.

Top 10 institutions on research of skeletal muscle ischemia-reperfusion injury.

Rank Institution Number of Publication % of Total Publication Global Rank Country
1 Harvard University 118 3.2 4 USA
2 University of Toronto 58 1.58 41 Canada
3 University of California San Diego 51 1.39 301 USA
4 University of Western Ontario 41 1.11 597 Canada
5 Duke University 38 1.03 79 USA
6 University of Nevada 38 1.03 2135 USA
7 University of Florida 37 1 137 USA
8 Brigham and Women's Hospital 36 0.98 84 USA
9 Louisiana State University 35 0.95 2546 USA
10 Universidade de Sao Paulo 33 0.9 50 Brazil
Open in a new tab

Fig. 4.

Fig. 4

Open in a new tab

Visualization analysis of institutions. Node size is proportional to the number of publications by the institution, and the thickness of the connecting line between the nodes is the strength of the institution's co-operation. Different colors represent clusters with different affinities.

3.3. Authors and co-cited authors

We observed that 16,132 authors are involved in studying skeletal muscle I/R injury. Among the top 10 authors, 3 published at least 20 papers each (Table 3). Our collaborative network based on authors having ≥3 publications (Fig. 5A) revealed that Hobson RW, Hechtman HB, Korthuis RJ, Moore FD, and Duran WN had the most prominent nodes as they published the most related articles. Authors from the same country collaborated more often and were more closely connected. However, there was little collaboration between authors from different countries.

Table 3.

Top 10 authors and co-cited authors on research of skeletal muscle ischemia-reperfusion injury.

Rank Author Affiliations Number of Publication Co-Cited Authors Affiliations Citations
1 Hobson RW UMDNJ-New Jersey Medical School 25 Korthuis RJ Louisiana State University 451
2 Hechtman HB Brigham and Women's Hospital 23 Wang WZ University of Nevada School of Medicine 436
3 Korthuis RJ Louisiana State University 20 Menger MD University of Saarland 365
4 Moore FD Brigham and Women's Hospital 19 Granger DN Louisiana State University 329
5 Duran WN UMDNJ-New Jersey Medical School 13 Pang CY University of Toronto 313
6 Austen WG Massachusetts General Hospital 12 Murry CE Duke University 294
7 Freischlag JA Medical College of Wisconsin 12 Blaisdell FW University California Davis Medical Center 279
8 Walker PM University of Toronto 12 Hausenloy DJ University College London 275
9 Kobzik L Brigham and Women's Hospital 11 Mccord JM University of Colorado 273
10 Cambria RA UMDNJ-New Jersey Medical School 10 Carden DL Louisiana State University 258
Open in a new tab

Fig. 5.

Fig. 5

Open in a new tab

Visualization analysis of authors. (A) Network visualization mapping of authors. (B) Network visualization mapping of co-cited Authors. The size of the nodes corresponds to the number of publications authored by each individual, while the thickness of the connecting lines between nodes indicates the intensity of collaboration among authors. Nodes of different colors denote authors belonging to distinct clusters.

Five of the 73,326 co-cited authors had more than 300 co-citations (Table 3). The author with the highest number of co-citations was Korthuis RJ (n = 451), followed by Wang WZ (n = 436) and Menger MD (n = 365). Authors with at least 30 co-citations were filtered to plot the co-citation network (Fig. 5B). Fig. 5B shows active collaboration between co-cited authors, such as Korthuis RJ, Wang WZ, and Menger MD.

3.4. Journals and co-cited journals

Studies on skeletal muscle I/R injury have been published in 962 journals. The top 20 journals publishing research articles and reviews on skeletal muscle I/R injury are listed in Table 4. The top three journals are the Journal of Surgical Research (IF 2.2), the American Journal of Physiology-Heart and Circulatory Physiology (IF 4.8), and Plastic and Reconstructive Surgery (IF 3.6). Nine of the top 20 journals showed a JCR quartile ranking of Q1, thus indicating that these journals have a high academic reputation in the field. In terms of the number of co-citations among the top 20 journals, the Journal of Biological Chemistry (Co-citation = 5319), Circulation (Co-citation = 5262), Circulation Research (Co-citation = 4572) and American Journal of Physiology (Co-citation = 4309) were cited more than 4000 times (Table 5). Nature had the highest impact factor (IF = 64.8), followed by Science (IF = 56.9). We constructed a collaborative network based on journals with published papers greater than or equal to 20 (Fig. 6A). Fig. 6A shows that the Journal of Surgical Research has active citation relationships with the Journal of Vascular Surgery, Plastic and Reconstructive Surgery, and the American Journal of Physiology-Heart and Circulatory Physiology. For better visualization of the co-citation relationship between journals, the collaborative network constructed for journals with more than 100 citations was classified into four categories (Fig. 6B). Articles from journals within the same category are more likely to have a similar research orientation or a specific internal logic [30]. For example, the Journal of Biological Chemistry and Circulation Research, Circulation, and American Journal of Physiology has a strong co-citation relationship because they focus on the pathophysiological processes and molecular mechanisms of skeletal muscle ischemia-reperfusion injury.

Table 4.

Top 20 journals on research of skeletal muscle ischemia-reperfusion injury.

Rank Journal Number of Publication Country Impact Factor (2022) JCR Quartile (2022) H-Index (2022)
1 Journal of Surgical Research 143 USA 2.2 Q2 177
2 American Journal of Physiology - Heart and Circulatory Physiology 106 USA 4.8 Q2 216
3 Plastic and Reconstructive Surgery 72 USA 3.6 Q1 198
4 Journal of Applied Physiology 71 USA 3.3 Q2 251
5 Microsurgery 62 USA 2.1 Q2 70
6 Journal of Vascular Surgery 50 USA 4.3 Q2 210
7 PLoS ONE 46 USA 3.7 Q2 404
8 Journal of Reconstructive Microsurgery 44 USA 2.1 Q2 61
9 Journal of Molecular and Cellular Cardiology 41 USA 5.0 Q2 169
10 Free Radical Biology and Medicine 39 USA 7.4 Q1 289
11 Annals of Plastic Surgery 39 USA 1.5 Q3 101
12 American Journal of Physiology - Regulatory Integrative and Comparative Physiology 36 USA 2.8 Q2 189
13 Frontiers in Physiology 34 Switzerland 4.0 Q2 140
14 Circulation Research 33 USA 20.1 Q1 369
15 International Journal of Molecular Sciences 33 Switzerland 5.6 Q1 230
16 Cardiovascular Research 32 USA 10.9 Q1 234
17 Circulation 31 USA 37.8 Q1 654
18 American Journal of Physiology 31 USA 3.0 Q1 82
19 European Journal of Vascular and Endovascular Surgery 27 England 5.7 Q1 133
20 Journal of Orthopaedic Research 25 USA 2.8 Q2 168
Open in a new tab

Table 5.

Top 20 co-cited journals on research of skeletal muscle ischemia-reperfusion injury.

Rank Co-cited Journal Cited Number Country Impact Factor (2022) JCR Quartile (2022) H-Index (2022)
1 Journal of Biological Chemistry 5319 USA 4.8 Q2 544
2 Circulation 5262 USA 37.8 Q1 654
3 Circulation Research 4572 USA 20.1 Q1 369
4 American Journal of Physiology 4309 USA 3.0 Q1 82
5 American Journal of Physiology - Heart and Circulatory Physiology 3833 USA 4.8 Q2 216
6 Journal of Applied Physiology 3336 USA 3.3 Q2 251
7 Proceedings of the National Academy of Sciences of the United States of America 3118 USA 11.1 Q1 838
8 Journal of Surgical Research 2674 USA 2.2 Q2 177
9 Cardiovascular Research 2628 England 10.9 Q1 234
10 Journal of Clinical Investigation 2626 USA 15.9 Q1 527
11 Journal of Molecular and Cellular Cardiology 2261 USA 5.0 Q2 169
12 Plastic and Reconstructive Surgery 2186 USA 3.6 Q1 198
13 Nature 1898 England 64.8 Q1 1331
14 Free Radical Biology and Medicine 1785 USA 7.4 Q1 289
15 Journal of Vascular Surgery 1613 USA 4.3 Q2 210
16 Journal of Physiology 1469 England 5.5 Q1 261
17 Science 1445 USA 56.9 Q1 1283
18 PLoS ONE 1383 USA 3.7 Q2 404
19 faseb j 1380 USA 4.8 Q2 297
20 Biochemical and Biophysical Research Communications 1304 USA 3.1 Q3 282
Open in a new tab

Fig. 6.

Fig. 6

Open in a new tab

Visualization analysis of journals. (A) The network visualization of journals. (B) The network visualization of co-cited journals. Node size is proportional to the number of journal publications, and the thickness of the connecting lines between nodes is the citation strength between journals. Each node's color corresponds to a cluster, with different hues representing distinct clusters. (C) Dual-map overlay of journals on research of skeletal muscle ischemia/reperfusion injury. The citing journals collection is on the left, the cited journals collection is on the right, and the colored paths indicate the citation relationships. The four main citation paths are marked in orange and green, representing studies published in Molecular/Biology/Immunology and Medicine/Medical/Clinical journals primarily cited by Molecular/Biology/Genetics and Health/Nursing/Medicine journals.

The average IF (p = 0.021) and H-index (p = 0.005) of the top 20 co-cited journals were higher than the top 20 journals regarding the number of publications. However, the JCR quartile did not differ significantly between the two (p = 0.623) (Table 6).

Table 6.

Analysis comparing top 20 journals with top 20 co-cited journals on impact factor, JCR quartile and H-index.

Top 20 journals Top 20 co-cited journals p Value
Impact Factor (2022) 6.64 ± 8.43 13.65 ± 18.20 0.021*
JCR Quartile (2022) 0.623
 Q1 8 11
 Q2 11 8
 Q3 1 1
H-Index (2021) 217.25 ± 136.49 430.80 ± 351.12 0.005*
Open in a new tab

A dual-map overlay of journals generated with CiteSpace was used to study the citation relationships between journals and cited journals. The map showed clusters of cited journals on the left, clusters of co-cited journals on the right, and sample waves from left to right showing citation associations represented by colored paths [31]. The four main citation paths are marked in orange and green, representing studies published in Molecular/Biology/Immunology and Medicine/Medical/Clinical journals primarily cited by Molecular/Biology/Genetics and Health/Nursing/Medicine journals, as shown in Fig. 6.

3.5. Co-cited references and references with citation bursts

Over the past 37 years of research, 118657 references have been made to the literature on skeletal muscle I/R injury. The top 20 co-cited references (Table 7) had a minimum citation of 75, and the top two were cited more than 200 times. We selected the literature with more than or equal to 30 citations to construct the co-citation network graph (Fig. 7A).

Table 7.

Top 20 co-cited articles on research of skeletal muscle ischemia-reperfusion injury.

Rank Co-cited reference Journal
Citations Year Name Country Impact Factor (2022) JCR Quartile (2022) H-Index (2022)
1 Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium 258 1986 Circulation USA 37.8 Q1 654
2 The pathophysiology of skeletal muscle ischemia and the reperfusion syndrome: a review 234 2002 Cardiovascular Surgery USA – – –
3 The role of oxygen-derived free radicals in ischemia-induced increases in canine skeletal muscle vascular permeability 192 1985 Circulation Research USA 20.1 Q1 369
4 Oxygen-derived free radicals in postischemic tissue injury 190 1985 New England Journal of Medicine USA 158.5 Q1 1130
5 Leukocyte depletion attenuates vascular injury in postischemic skeletal muscle 139 1988 American Journal of Physiology USA 3.0 Q1 82
6 Neutrophil-mediated microvascular dysfunction in postischemic canine skeletal muscle. Role of granulocyte adherence 124 1990 Circulation Research USA 20.1 Q1 369
7 Protein measurement with the Folin phenol reagent 112 1951 Journal of Biological Chemistry USA 4.8 Q2 544
8 Inflammatory responses to ischemia and reperfusion in skeletal muscle 105 1998 Molecular and Cellular Biochemistry USA 4.2 Q2 132
9 Acute ischaemic preconditioning protects against skeletal muscle infarction in the pig 100 1995 Cardiovascular Research England 10.9 Q1 234
10 Metabolic response of skeletal muscle to ischemia 88 1986 American Journal of Physiology USA 3.0 Q1 82
11 Role of neutrophils in ischemia-reperfusion-induced microvascular injury 87 1987 American Journal of Physiology USA 3.0 Q1 82
12 Free radical defense mechanisms and neutrophil infiltration in postischemic skeletal muscle 86 1989 American Journal of Physiology USA 3.0 Q1 82
13 Reperfusion injury of ischemic skeletal muscle is mediated by natural antibody and complement 85 1996 Journal of Experimental Medicine USA 15.3 Q1 478
14 Ischemia-reperfusion injury 83 1994 British Journal of Surgery England 9.6 Q1 219
15 Salvage of skeletal muscle with free radical scavengers 79 1987 Journal of Vascular Surgery USA 4.3 Q2 210
16 Pathophysiology of ischemia-reperfusion injury 78 2000 Journal of Pathology England 7.3 Q1 297
17 Tissue destruction by neutrophils 76 1989 New England Journal of Medicine USA 158.5 Q1 1130
18 Pathophysiology of ischemia reperfusion injury: central role of the neutrophil 76 1991 British Journal of Surgery England 9.6 Q1 219
19 Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury 75 1988 American Journal of Physiology USA 3.0 Q1 82
20 Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog 75 1983 Circulation USA 37.8 Q1 654
Open in a new tab

Fig. 7.

Fig. 7

Open in a new tab

Visualization analysis of co-cited references. (A) The network visualization of co-cited references. Each node represents a reference, where the node's size represents the citation counts, and each link between references indicates that the two references were co-cited, with a thicker line indicating a closer relationship. (B) Top 25 references with the strongest citation bursts. The blue bars indicate references that have been published, and the red bars indicate citation bursts.

Citation burst studies indicate the most active area of research frequently cited by scholars in a given field over time. It reflects emerging academic trends and new topics, predicts frontier directions, and reveals potential hotspots in a field. CiteSpace analysis identified the top 25 research articles with citation bursts (Fig. 7B). The earliest citation burst occurred in 1987, and the most recent citation burst was in 2018, as shown in Fig. 7B. The burst intensity of the top 25 references ranged from 9.99 to 24.73, and the endurance intensity was from 2 to 5 years. Our analysis indicated that the current research focuses on studying the primary sources of ROS production in skeletal muscle during ischemia-reperfusion, the mechanisms of mitochondrial dysfunction in skeletal muscle I/R, and the effects of I/R injury on different muscle phenotypes.

3.6. Analysis of keywords

Keyword analysis is used to determine the research hotspots in a particular field. We used VOSviewer to perform a co-occurrence analysis and found 11770 keywords. These keywords were further classified into six categories with the help of a collaborative network constructed with keywords having more than 20 occurrences (Fig. 8A). The most prominent keywords that emerged were Skeletal muscle (red), Ischemia-reperfusion (yellow), Mitochondrial dysfunction (green), Mechanistic studies (dark blue), Oxidative stress (purple), and Therapeutic modalities (light blue). The top 20 high-frequency keywords in skeletal muscle I/R research are listed in Table 8. Excluding skeletal muscle and ischemia-reperfusion-related keywords, oxidative stress, expression, rat, activation, nitric-oxide, heart, model, inflammation, microcirculation, apoptosis, and exercise appeared at least 170 times. The top 25 keywords with the highest burst intensity are shown in Fig. 8B. We found that free radical (26.58), xanthine oxidase (26.34), and neutrophil (22.73) had the highest burst intensity. The keyword with the most prolonged outbreak was free radical, which lasted 17 years from 1987 to 2004. Interestingly, the three keywords apoptosis, pathway, and oxidative stress showed a recent (2014–2023) outbreak of citations, suggesting that the studies on the mechanisms of skeletal muscle I/R injury may be a hot spot for future research.

Fig. 8.

Fig. 8

Open in a new tab

Visualization analysis of keywords. (A) Network visualization mapping of the keywords. The nodes represent keywords, and their size is proportional to the frequency of the keywords. The nodes and lines of different colors symbolize diverse keyword clusters. (B) Top 25 keywords with the strongest citation bursts. Red and bold horizontal bars indicate hot spots with the strongest citation bursts. (C) Timeline view of the 10 clusters of the co-occurrence keywords. Each horizontal line indicates a cluster. The size of the circle indicates the frequency of occurrence, with the most recently established links in yellow. (D) Three-field plot of analysis authors, keywords, and journals on the research of skeletal muscle ischemia/reperfusion injury (middle field: keywords; left field: authors; right field: journals).

Table 8.

Top 20 keywords on research of skeletal muscle ischemia-reperfusion injury.

Rank Keywords Occurrences Rank Keywords Occurrences
1 skeletal-muscle 1576 11 expression 281
2 ischemia 692 12 rat 268
3 ischemia-reperfusion injury 669 13 activation 267
4 reperfusion injury 655 14 nitric-oxide 254
5 reperfusion 593 15 heart 221
6 injury 436 16 model 201
7 oxidative stress 431 17 inflammation 187
8 ischemia-reperfusion 360 18 microcirculation 186
9 skeletal muscle 327 19 apoptosis 182
10 ischemia/reperfusion injury 304 20 exercise 178
Open in a new tab

We also mapped a timeline view of skeletal muscle I/R injury research keywords using CiteSpace (Fig. 8C) to study the emergence, prevalence, and decline of hotspots over the period and research progression of each cluster (i.e., subfield) [31]. A total of 10 clusters were identified: fatty acid oxidation, angiogenesis, monoclonal antibody, reperfusion injury, oxidative stress, near-infrared spectroscopy, injury, creatine kinase, protein synthesis, and strength training (Table 9). Except for protein synthesis and strength training (#8 and #9), the other eight clusters pointed towards the main research interest, with #0 (fatty acid oxidation) being the largest cluster, followed by #1 (angiogenesis) and #2 (monoclonal antibody).

Table 9.

Cluster summary of keywords time line view.

Cluster ID Size Silhouette Mean (Year) Cluster lable
0 175 0.568 2008 fatty acid oxidation
1 155 0.587 2009 angiogenesis
2 152 0.642 1995 monoclonal antibody
3 139 0.562 2003 reperfusion injury
4 119 0.693 2002 oxidative stress
5 116 0.677 1999 near-infrared spectroscopy
6 38 0.881 2008 injury
7 22 0.903 2001 creatine kinase
8 6 0.973 1998 protein synthesis
9 3 0.987 2016 strength training
Open in a new tab

A three-field plot that describes the relationship between the principal elements by the strength of the connecting links [28] was plotted with authors, keywords, and journals as the main elements (Fig. 8D). Our result showed that “skeletal muscle” and “mitochondria” were the most frequently used keywords. The authors, Wang WZ and Zamboni WA, had a relatively strong association with the keywords “skeletal muscle” and “muscle”. The Journal of Surgical Research and American Journal of Physiology-Heart and Circulatory Physiology covered the most high-frequency keywords.

4. Discussion

Over the past few decades, researchers have made tremendous efforts to study skeletal muscle ischemia-reperfusion injury and have made significant progress in its treatment (Fig. 9). In this study, we did a bibliometric analysis of the research publications over 37 years on skeletal muscle I/R injury to (1) assess the involvement of country, institution, author, impact, and their collaboration with each other, (2) map areas of knowledge, and (3) identify research hotspots and emerging trends. Our findings provide a solid foundation for exploring the body of knowledge in the field of skeletal muscle I/R injury.

Fig. 9.

Fig. 9

Open in a new tab

Timeline of part of landmark achievements in skeletal muscle ischemia/reperfusion injury.

4.1. General information

One indicator of a field's development direction is the yearly variation in production output. According to the WoSCC database, 16132 authors from 2846 institutions in 83 countries/regions published 3682 articles or reviews on ischemia-reperfusion injury in 962 scientific journals. With the first articles being published in 1986, we observed that the general trend until 2023 is a slow but steady growth of the knowledge base. The top 10 countries contributing to research on ischemia-reperfusion injury were the developed countries except for China and Turkey. The USA contributed more than 1/3rd (36.23 %) of the total publications, with the highest H-index, and about 70 % of the top 10 research institutions, indicating the USA has a positive academic influence on skeletal muscle I/R. Our study also showed significant research collaborations between the USA and European countries, while there are relatively few collaborations in Asian countries. Despite having the second-highest number of publications, none of the Chinese institutions made it to the top 10 research institutions. This indicates that there is relative fragmentation of research in China. The Harvard University of USA emerged as the most active collaborator in studying skeletal muscle ischemia-reperfusion injury. A high level of co-operation between countries and institutions is vital for high-quality research results. Therefore, researchers must strengthen their co-operation and exchanges with global institutions as research progresses to enhance their academic impact.

Our study showed that Hobson RW, Hechtman HB, and Korthuis RJ are the pioneers in this field, with at least 20 published articles each. Hobson RW and his group mainly studied the pathophysiological changes of skeletal muscle I/R injury and quantitative and qualitative assessment methods [[32], [33], [34], [35]], which laid a solid foundation for skeletal muscle I/R research. Korthuis RJ and his group published 20 articles with the highest citation frequency (Citation = 451). They mainly focused on intervention strategies for skeletal muscle I/R injury and related mechanisms [36], such as ischemic preconditioning prevents [[37], [38], [39]], inflammatory responses [40], CD18-dependent adherence [41], and adhesion molecule [42].

Journal of Surgical Research (IF = 2.2, Q2) had the highest number of published articles, indicating that it is currently the most sought-after journal in this area of research. The journal with the highest impact factor was Circulation (IF = 37.8, Q1). Most of the co-cited journals greatly impacted the Q1 JCR ranking. Comparing the IF and H-index of the top 20 journals regarding the number of publications and the top 20 co-cited journals, we found that the average IF (p = 0.021) and H-index (p = 0.005) of the top 20 co-cited journals were significantly high. Thus, the research articles published in these journals were internationally viewed, read, and referred to by researchers in this field and can be used to assess the current status and hot spots in I/R injury research. We further observed that studies on skeletal muscle I/R injury were mainly published in journals that mainly publish research papers on subjects related to Molecular, Biology, Immunology and Medicine, Medical, and Clinical, suggesting that the current research trend is mainly focused on understanding essential molecular as well as clinical aspect of I/R injury.

4.2. Knowledge base

Co-citation is literature cited by several other publications simultaneously. It is the basis of research in a particular field [31]. In this study, we selected the 20 most co-cited publications to determine the research base of skeletal muscle I/R. Murry CE et al. [43] published the most cited study in 1986, which showed that multiple brief ischemic preconditioning could ameliorate reperfusion injury. It laid the foundation for studying intervention strategies for I/R. To date, ischemic preconditioning remains a hot research topic in skeletal muscle I/R [44,45]. These top 20 most co-cited publications have focused on 1) the pathophysiology of skeletal muscle I/R, including the role of oxygen radicals, centrioles, antibody complement, inflammatory response, metabolic response, and xanthine oxidase; and 2) interventions for skeletal muscle I/R, such as ischemic preconditioning.

References with strong citation bursts are also used to characterize the research base of a field [31]. We identified the top 25 references with citation bursts using CiteSpace. The research article published by Blaisdell FW [1] in 2022 on the pathophysiology of skeletal muscle ischemia-reperfusion in Cardiovascular Surgery showed the strongest citation burst (intensity = 24.73) from 2004 to 2007. This indicates that research was mainly focused on skeletal muscle I/R pathophysiology during this period. The article with the longest duration of the citation burst was (2018–2023, intensity = 10.17), published by Charles AL et al. [46] in Frontiers in Physiology, 2017. They showed that glycolytic muscles are more prone to I/R than oxidation and suggested that muscle susceptibility is linked to muscle metabolic phenotypes, mainly muscle mitochondrial oxidative capacity. These results from our citation bursts study can be used by future researchers to locate studies that have made significant contributions to skeletal muscle I/R research.

4.3. Hotspots and frontiers

Keyword analysis helps to capture the core content and boundaries of a research field, and changes in keywords over time represent the evolution of the field [24]. Our bibliometric study showed that the dominant keywords were oxidative stress, expression, rat, activation, nitric oxide, model, inflammation, microcirculation, and apoptosis (Table 7). These keywords are closely related to the hot spots of research on skeletal muscle I/R mechanisms. The clustering analysis of keywords identified ten major subfields in skeletal muscle I/R research, and the timeline view showed the development of these subfields. We unfolded the analysis by highly explosive keywords, apoptosis, pathway, and oxidative stress, which had a recent (2014–2023) explosion of citations, indicating that the pathological mechanisms, molecular mechanisms, and downstream pathways of skeletal muscle I/R injury are the new research hotspots.

Apoptosis, defined as programmed cell death, was first proposed in 1972 by Kerr JF et al. [47] as distinct from necrosis. In recent decades, evidence from I/R models of the heart [48], liver [49], kidney [50], and brain [51] suggests that apoptosis is a major factor in I/R-induced cell death. However, the occurrence of apoptosis in skeletal muscle I/R injury remains controversial [52]. Knight KR et al. [53] found no indication of apoptosis in the nuclei of skeletal muscle fibers in a rat lower extremity tourniquet model. Wang WZ et al. [52] reported the presence of microscopic vascular endothelial cells in skeletal muscle of ischemia-reperfusion-induced apoptosis and concluded that necrosis was one of the major contributors. A recent study showed that FGF21 inhibited Drp1 activation and ameliorated I/R-induced apoptosis in skeletal muscle [54]. Another study showed that necrosis inhibitor-1 could ameliorate skeletal muscle I/R injury by regulating Bok-mediated apoptosis [55]. As research in this field has deepened, several types of programmed cell death have been proposed [[56], [57], [58], [59]]. The potential existence of additional death modes and their mechanisms in skeletal muscle ischemia-reperfusion (I/R) injury may be a promising direction for future studies.

Signaling pathways are a series of enzymatic reactions in which molecular signals from outside the cell are transmitted across the cell membrane to exert effects inside the cell. Studies have shown that multiple signaling pathways are involved in skeletal muscle I/R injury [60,61]. A genome-wide expression profiling study on skeletal muscle I/R injury in rats showed that mitogen-activated protein kinase (MAPK) and nuclear factor kappa-B (NF-κB) signaling pathways play an essential role in skeletal muscle I/R injury [60]. MAPK is a group of serine-activated proteins that can be activated by various extracellular stimuli, such as cytokines, neurotransmitters, hormones, cellular stress, and cell adhesion [62]. Zhu N et al. [63] found that Schisandrin B could ameliorate oxidative stress and inflammation by regulating p38MAPK and extracellular signal-regulated kinase (ERK) 1/2 in a rat hindlimb ischemia-reperfusion model. NF-κB is a dimeric redox-sensitive transcription factor composed of p50 and p65 that plays an essential role in ischemia-reperfusion injury [64]. NF-κB can be activated in various ways, releasing pro-inflammatory cytokines such as interleukin 6, interleukin 1, and tumor necrosis factor-alpha (TNF-α). Several studies have shown that inhibition of NF-κB is a potential intervention for treating I/R injury [[64], [65], [66]].

Oxidative stress is a state in which there is an imbalance between oxidative and antioxidant actions in the body. During skeletal muscle ischemia-reperfusion, large amounts of reactive oxygen species (ROS) are generated, which exceed the scavenging capacity of antioxidants, resulting in damage to proteins, lipids, and DNA [7]. Cheng et al. [67] showed that pterostilbene could attenuate oxidative stress damage in skeletal muscle caused by ischemia-reperfusion injury by activating silent information regulator 1 (SIRT1). Kuroda et al. [68] reported that 3-carbamoyl PROXYL-enhanced magnetic resonance imaging could effectively assess oxidative stress caused by skeletal muscle I/R, providing a basis for imaging assessment of oxidative stress.

Therefore, exploring the pathophysiological process of skeletal muscle I/R, in-depth molecular biology research, and mechanism exploration may be the hot spots and trends in the future.

5. Limitations

Utilizing three software programs: CiteSpace, VOSviewer, and R-bibliometrix, we conducted a systematic analysis of skeletal muscle I/R research trends, focal points, and advancements over the past 30 years, employing a bibliometric approach for the first time. However, there are several limitations to this study. Firstly, all literature utilized was sourced solely from the Web of Science. While the timely updates, authority, and breadth of the Web of Science facilitated the acquisition of extensive literature data to bolster our analysis, incorporating other databases could have potentially yielded additional relevant publications. Secondly, our study only encompassed research and review articles written in English, excluding non-English or non-research/review articles, which may have led to some omissions. Lastly, we would like to mention that as new studies are continuously emerging, we may have overlooked certain influential recently published works.

6. Conclusions

This study systematically reviewed more than thirty years of research in skeletal muscle I/R using bibliometric analysis to provide researchers with a holistic perspective. We found a significant increase in the number of articles published over the past two decades. Undoubtedly, the United States of America and China are the core centers of skeletal muscle I/R research. In terms of institutions, Harvard University is the leader in the field. Regarding authors, Hobson RW has the most output, while Korthuis RJ has the most impact and is widely cited. In terms of journals, the Journal of Surgical Research is the leading source of skeletal muscle I/R research, and the Journal of Biological Chemistry is the most cited. The pathophysiology, interventions, and molecular biological mechanisms of skeletal muscle I/R injury are the main research directions in this field. Apoptosis, signaling pathways, and oxidative stress are hot spots for future research. The results of this study provide a comprehensive bibliometric analysis of skeletal muscle I/R research from a global perspective, which may provide valuable clues for future research directions and scientific decisions in this field.

Ethics approval and consent to participate

Not applicable.

Consent for publication

All authors have read and approved the content and agree to submit for consideration for publication in the journal.

Data and code availability

The datasets generated and/or analysed during the current study are available in the [The Science Citation Index Expanded of Clarivate Analytics’S Web of Science Core Collection (WoSCC)] repository, https://www.webofscience.com/wos/alldb/basic-search. We have uploaded the search results in Appendix 1 of the supplementary materials.

Funding

This study was provided by Wuxi Top Medical Expert Team of “Taihu Talent Program” (TTPJY2021).

CRediT authorship contribution statement

Ming Zhou: Writing – original draft, Visualization, Software, Resources, Methodology, Formal analysis, Data curation, Conceptualization. Xueyuan Jia: Writing – original draft, Resources, Methodology, Formal analysis, Data curation. Hao Liu: Formal analysis, Data curation. Yuan Xue: Writing – review & editing, Validation. Yapeng Wang: Writing – review & editing, Validation. Zeqing Li: Writing – review & editing, Validation. Yongwei Wu: Writing – review & editing, Validation, Supervision, Project administration. Yongjun Rui: Writing – review & editing, Supervision, Project administration, Investigation, Funding acquisition, Conceptualization.

Declaration of competing interest

The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:Yongjun Rui reports financial support was provided by Wuxi Health Commission.

Acknowledgements

We thank Medjaden Inc. for the scientific editing of this manuscript.

We thank for my family and my wife Jie Gao who give me strength everywhere.

Footnotes

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.heliyon.2024.e37492.

Contributor Information

Yongwei Wu, Email: wuyongwei_trauma@163.com.

Yongjun Rui, Email: ryjwx_trauma@163.com.

Abbreviations

I/R

ischemia/reperfusion

WoSCC

Web of Science Core Collection

JCR

Journal Citation Report

IF

impact factor

H-index

Hirsch index

GDP

gross domestic product

MAPK

mitogen-activated protein kinase

NF-κB

nuclear factor kappa-B

ERK

extracellular signal-regulated kinase

TNF-α

tumor necrosis factor-alpha

SIRT1

silent information regulator 1

Appendix A. Supplementary data

The following is/are the supplementary data to this article:

mmc1.zip (10.2MB, zip)
mmc2.pdf (193.3KB, pdf)
mmc3.docx (443.7KB, docx)

References

  • 1.Blaisdell F.W. The pathophysiology of skeletal muscle ischemia and the reperfusion syndrome: a review. Cardiovasc. Surg. 2002;10:620–630. doi: 10.1016/s0967-2109(02)00070&#x02013;00074. [DOI] [PubMed] [Google Scholar]
  • 2.Leurcharusmee P., Sawaddiruk P., Punjasawadwong Y., Chattipakorn N., Chattipakorn S.C. The possible pathophysiological outcomes and mechanisms of tourniquet-induced ischemia-reperfusion injury during total knee arthroplasty. Oxid. Med. Cell. Longev. 2018:8087598. doi: 10.1155/2018/8087598. 2018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Wang W.Z., Baynosa R.C., Zamboni W.A. Update on ischemia-reperfusion injury for the plastic surgeon: 2011. Plast. Reconstr. Surg. 2011;128:685e–692e. doi: 10.1097/PRS.0b013e318230c57b. [DOI] [PubMed] [Google Scholar]
  • 4.Paradis S., Charles A.L., Meyer A., et al. Chronology of mitochondrial and cellular events during skeletal muscle ischemia-reperfusion. Am. J. Physiol.: Cell Physiol. 2016;310:C968–C982. doi: 10.1152/ajpcell.00356.2015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Watanabe M., Kamimura N., Iuchi K., et al. Protective effect of hydrogen gas inhalation on muscular damage using a mouse hindlimb ischemia-reperfusion injury model. Plast. Reconstr. Surg. 2017;140:1195–1206. doi: 10.1097/PRS.0000000000003878. [DOI] [PubMed] [Google Scholar]
  • 6.Apichartpiyakul P., Shinlapawittayatorn K., Rerkasem K., Chattipakorn S.C., Chattipakorn N. Mechanisms and interventions on acute lower limb ischemia/reperfusion injury: a review and insights from cell to clinical investigations. Ann. Vasc. Surg. 2022;86:452–481. doi: 10.1016/j.avsg.2022.04.040. [DOI] [PubMed] [Google Scholar]
  • 7.Zhou T., Prather E.R., Garrison D.E., Zuo L. Interplay between ROS and antioxidants during ischemia-reperfusion injuries in cardiac and skeletal muscle. Int. J. Mol. Sci. 2018;19 doi: 10.3390/ijms19020417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Barnig C., Lutzweiler G., Giannini M., et al. Resolution of inflammation after skeletal muscle ischemia-reperfusion injury: a focus on the lipid mediators lipoxins, resolvins. Protectins and Maresins, Antioxidants. 2022;11 doi: 10.3390/antiox11061213. Basel. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Soares R.O.S., Losada D.M., Jordani M.C., Evora P., Castro E.S.O. Ischemia/reperfusion injury revisited: an overview of the latest pharmacological strategies. Int. J. Mol. Sci. 2019;20 doi: 10.3390/ijms20205034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Zhou M., Zhang H., Chen H., Qi B. Adiponectin protects skeletal muscle from ischaemia-reperfusion injury in mice through miR-21/PI3K/Akt signalling pathway. Int. Wound J. 2023;20:1647–1661. doi: 10.1111/iwj.14022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Wang H., Shi J., Shi S., et al. Bibliometric analysis on the progress of chronic heart failure. Curr. Probl. Cardiol. 2022;47:101213. doi: 10.1016/j.cpcardiol.2022.101213. [DOI] [PubMed] [Google Scholar]
  • 12.Wilson M., Sampson M., Barrowman N., Doja A. Bibliometric analysis of neurology articles published in general medicine journals. JAMA Netw. Open. 2021;4 doi: 10.1001/jamanetworkopen.2021.5840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Zhang Q., Zeng Y., Zheng S., et al. Research hotspots and frotiers of stem cells in stroke: a bibliometric analysis from 2004 to 2022. Front. Pharmacol. 2023;14:1111815. doi: 10.3389/fphar.2023.1111815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Wu F., Gao J., Kang J., et al. Knowledge mapping of exosomes in autoimmune diseases: a bibliometric analysis (2002-2021) Front. Immunol. 2022;13:939433. doi: 10.3389/fimmu.2022.939433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.He Z., Dai L., Zuo Y., et al. Hotspots and frontiers in pulmonary arterial hypertension research: a bibliometric and visualization analysis from 2011 to 2020. Bioengineered. 2022;13:14667–14680. doi: 10.1080/21655979.2022.2100064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Ahmad P., Slots J. A bibliometric analysis of periodontology. Periodontol. 2000. 2021;85:237–240. doi: 10.1111/prd.12376. [DOI] [PubMed] [Google Scholar]
  • 17.Okewunmi J., Kiani S.N., Poeran J., Galatz L.M. Female authorship in the US orthopaedics literature: a bibliometric analysis of trends. J. Am. Acad. Orthop. Surg. 2023 doi: 10.5435/JAAOS-D-22-00918. [DOI] [PubMed] [Google Scholar]
  • 18.Tong X.F., Xiao Z.Y., Li P.T., et al. Angiogenesis and flap-related research: a bibliometric analysis. Int. Wound J. 2023 doi: 10.1111/iwj.14181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Carter-Templeton H., Frazier R.M., Wu L. T HW, robotics in nursing: a bibliometric analysis. J. Nurs. Scholarsh. 2018;50:582–589. doi: 10.1111/jnu.12399. [DOI] [PubMed] [Google Scholar]
  • 20.Liu Y., Jitpakdee K., Van Isseldyk F., et al. Bibliometric analysis and description of research trends on transforaminal full-endoscopic approach on the spine for the last two-decades. Eur. Spine J. 2023 doi: 10.1007/s00586-023-07661-0. [DOI] [PubMed] [Google Scholar]
  • 21.Liao J., Yu X., Chen J., et al. Knowledge mapping of autophagy in osteoarthritis from 2004 to 2022: a bibliometric analysis. Front. Immunol. 2023;14:1063018. doi: 10.3389/fimmu.2023.1063018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Liu S., Song L., Dai W., et al. Worldwide productivity and research trend of publications concerning electroactive materials and spinal cord injury: a bibliometric study. Front. Bioeng. Biotechnol. 2023;11:1094059. doi: 10.3389/fbioe.2023.1094059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Brandt J.S., Hadaya O., Schuster M., et al. A bibliometric analysis of top-cited journal articles in obstetrics and gynecology. JAMA Netw. Open. 2019;2 doi: 10.1001/jamanetworkopen.2019.18007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Dong Y., Yao J., Deng Q., et al. Relationship between gut microbiota and rheumatoid arthritis: a bibliometric analysis. Front. Immunol. 2023;14:1131933. doi: 10.3389/fimmu.2023.1131933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.van Eck N.J., Waltman L. Software survey: VOSviewer, a computer program for bibliometric mapping. Scientometrics. 2010;84:523–538. doi: 10.1007/s11192-009-0146-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Chen C., Hu Z., Liu S., Tseng H. Emerging trends in regenerative medicine: a scientometric analysis in CiteSpace. Expet Opin. Biol. Ther. 2012;12:593–608. doi: 10.1517/14712598.2012.674507. [DOI] [PubMed] [Google Scholar]
  • 27.Chen C. A glimpse of the first eight months of the COVID-19 literature on Microsoft academic graph: themes, citation contexts, and uncertainties. Front Res Metr Anal. 2020;5:607286. doi: 10.3389/frma.2020.607286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Aria M., Cuccurullo C., Egghe L. bibliometrix, An R-tool for comprehensive science mapping analysis. Journal of Informetrics. 2017;11:959–975. doi: 10.1016/j.joi.2017.08.007. [DOI] [Google Scholar]
  • 29.Quaia E., Vernuccio F. The H index myth: a form of fanaticism or a simple misconception? Tomography. 2022;8:1241–1243. doi: 10.3390/tomography8030102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Chen S., Kong J., Feng L. The trend of drug therapy on uveitic macular edema: a bibliometric analysis of the 100 most cited articles. Front. Med. 2022;9:807319. doi: 10.3389/fmed.2022.807319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Chen C. Science mapping: a systematic review of the literature, Journal of Data and Information Science. 2017;2:1–40. [Google Scholar]
  • 32.Suval W.D., Duran W.N., Boric M.P., et al. Microvascular transport and endothelial cell alterations preceding skeletal muscle damage in ischemia and reperfusion injury. Am. J. Surg. 1987;154:211–218. doi: 10.1016/0002-9610(87)90181&#x02013;90184. [DOI] [PubMed] [Google Scholar]
  • 33.Belkin M., Brown R.D., Wright J.G., LaMorte W.W., Hobson R.W., 2nd A new quantitative spectrophotometric assay of ischemia-reperfusion injury in skeletal muscle. Am. J. Surg. 1988;156:83–86. doi: 10.1016/s0002-9610(88)80360-x. [DOI] [PubMed] [Google Scholar]
  • 34.Blebea J., Kerr J.C., Shumko J.Z., Feinberg R.N., Hobson R.W., 2nd Quantitative histochemical evaluation of skeletal muscle ischemia and reperfusion injury. J. Surg. Res. 1987;43:311–321. doi: 10.1016/0022-4804(87)90087&#x02013;4. [DOI] [PubMed] [Google Scholar]
  • 35.Suval W.D., Hobson R.W., 2nd, Boric M.P., Ritter A.B., Duran W.N. Assessment of ischemia reperfusion injury in skeletal muscle by macromolecular clearance. J. Surg. Res. 1987;42:550–559. doi: 10.1016/0022-4804(87)90031-x. [DOI] [PubMed] [Google Scholar]
  • 36.Rubin B.B., Romaschin A., Walker P.M., Gute D.C., Korthuis R.J. Mechanisms of postischemic injury in skeletal muscle: intervention strategies. J. Appl. Physiol. 1996;80:369–387. doi: 10.1152/jappl.1996.80.2.369. [DOI] [PubMed] [Google Scholar]
  • 37.Akimitsu T., Gute D.C., Korthuis R.J. Ischemic preconditioning attenuates postischemic leukocyte adhesion and emigration. Am. J. Physiol. Heart Circ. Physiol. 1996;271:H2052–H2059. doi: 10.1152/ajpheart.1996.271.5.H2052. [DOI] [PubMed] [Google Scholar]
  • 38.Dayton C., Yamaguchi T., Warren A., Korthuis R.J. Ischemic preconditioning prevents postischemic arteriolar, capillary, and postcapillary venular dysfunction: signaling pathways mediating the adaptive metamorphosis to a protected phenotype in preconditioned endothelium. Microcirculation. 2002;9:73–89. doi: 10.1038/sj.mn.7800122. [DOI] [PubMed] [Google Scholar]
  • 39.Ishida T., Yarimizu K., Gute D.C., Korthuis R.J. Mechanisms of ischemic preconditioning. Shock. 1997;8:86–94. doi: 10.1097/00024382-199708000-00003. [DOI] [PubMed] [Google Scholar]
  • 40.Gute D.C., Ishida T., Yarimizu K., Korthuis R.J. Inflammatory responses to ischemia and reperfusion in skeletal muscle. Mol. Cell. Biochem. 1998;179:169–187. doi: 10.1023/a:1006832207864. [DOI] [PubMed] [Google Scholar]
  • 41.Jerome S.N., Smith C.W., Korthuis R.J. CD18-dependent adherence reactions play an important role in the development of the no-reflow phenomenon. Am. J. Physiol. 1993;264:H479–H483. doi: 10.1152/ajpheart.1993.264.2.H479. [DOI] [PubMed] [Google Scholar]
  • 42.Korthuis R.J., Gute D.C. Adhesion molecule expression in postischemic microvascular dysfunction: activity of a micronized purified flavonoid fraction. J. Vasc. Res. 1999;36:15–23. doi: 10.1159/000054070. [DOI] [PubMed] [Google Scholar]
  • 43.Murry C.E., Jennings R.B., Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74:1124–1136. doi: 10.1161/01.cir.74.5.1124. [DOI] [PubMed] [Google Scholar]
  • 44.Morikawa T., Shimasaki M., Ichiseki T., et al. The possibility of IPC to prevent ischemic-reperfusion injury in skeletal muscle in a rat. J. Clin. Med. 2023;12 doi: 10.3390/jcm12041501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Guillot M., Charles A.L., Lejay A., et al. Deleterious effects of remote ischaemic per-conditioning during lower limb ischaemia-reperfusion in mice. Eur. J. Vasc. Endovasc. Surg. 2021;62:953–959. doi: 10.1016/j.ejvs.2021.06.032. [DOI] [PubMed] [Google Scholar]
  • 46.Charles A.L., Guilbert A.S., Guillot M., et al. Muscles susceptibility to ischemia-reperfusion injuries depends on fiber type specific antioxidant level. Front. Physiol. 2017;8:52. doi: 10.3389/fphys.2017.00052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Kerr J.F., Wyllie A.H., Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 1972;26:239–257. doi: 10.1038/bjc.1972.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Qian W., Liu D., Han Y., et al. Cyclosporine A-loaded apoferritin alleviates myocardial ischemia-reperfusion injury by simultaneously blocking ferroptosis and apoptosis of cardiomyocytes. Acta Biomater. 2023;160:265–280. doi: 10.1016/j.actbio.2023.02.025. [DOI] [PubMed] [Google Scholar]
  • 49.Zhang S., Tang J., Sun C., et al. Dexmedetomidine attenuates hepatic ischemia-reperfusion injury-induced apoptosis via reducing oxidative stress and endoplasmic reticulum stress. Int. Immunopharm. 2023;117:109959. doi: 10.1016/j.intimp.2023.109959. [DOI] [PubMed] [Google Scholar]
  • 50.Zhang B., Wan S., Liu H., et al. Naringenin alleviates renal ischemia reperfusion injury by suppressing ER stress-induced pyroptosis and apoptosis through activating Nrf2/HO-1 signaling pathway. Oxid. Med. Cell. Longev. 2022;2022:5992436. doi: 10.1155/2022/5992436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Fu J., Yu L., Yu Q., et al. Ginsenoside compound K reduces ischemia/reperfusion-induced neuronal apoptosis by inhibiting PTP1B-mediated IRS1 tyrosine dephosphorylation. J Ginseng Res. 2023;47:274–282. doi: 10.1016/j.jgr.2022.08.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Wang W.Z., Fang X.H., Stephenson L.L., Khiabani K.T., Zamboni W.A. Ischemia-reperfusion-induced apoptotic endothelial cells isolated from rat skeletal muscle. Plast. Reconstr. Surg. 2009;123:131S–138S. doi: 10.1097/PRS.0b013e318191c584. [DOI] [PubMed] [Google Scholar]
  • 53.Knight K.R., Messina A., Hurley J.V., et al. Muscle cells become necrotic rather than apoptotic during reperfusion of ischaemic skeletal muscle. Int. J. Exp. Pathol. 1999;80:169–175. doi: 10.1046/j.1365-2613.1999.00111.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Li B., Liu L. Fibroblast growth factor 21, a stress regulator, inhibits Drp1 activation to alleviate skeletal muscle ischemia/reperfusion injury. Lab. Invest. 2022;102:979–988. doi: 10.1038/s41374-022-00787-7. [DOI] [PubMed] [Google Scholar]
  • 55.Cao Y., Wang H.B., Ni C.J., et al. Necrostatin-1 prevents skeletal muscle ischemia reperfusion injury by regulating Bok-mediated apoptosis. J. Chin. Med. Assoc. 2023;86:26–33. doi: 10.1097/JCMA.0000000000000806. [DOI] [PubMed] [Google Scholar]
  • 56.Liu Y., Zhang J., Zhang D., et al. Research progress on the role of pyroptosis in myocardial ischemia-reperfusion injury. Cells. 2022;11 doi: 10.3390/cells11203271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Popov S.V., Mukhomedzyanov A.V., Voronkov N.S., et al. Regulation of autophagy of the heart in ischemia and reperfusion. Apoptosis. 2023;28:55–80. doi: 10.1007/s10495-022-01786-1. [DOI] [PubMed] [Google Scholar]
  • 58.Maslov L.N., Popov S.V., Naryzhnaya N.V., et al. The regulation of necroptosis and perspectives for the development of new drugs preventing ischemic/reperfusion of cardiac injury. Apoptosis. 2022;27:697–719. doi: 10.1007/s10495-022-01760-x. [DOI] [PubMed] [Google Scholar]
  • 59.Zhou L., Han S., Guo J., et al. Ferroptosis-A new dawn in the treatment of organ ischemia-reperfusion injury. Cells. 2022;11 doi: 10.3390/cells11223653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Chang N.J., Weng W.H., Chang K.H., et al. Genome-wide gene expression profiling of ischemia-reperfusion injury in rat kidney, intestine and skeletal muscle implicate a common involvement of MAPK signaling pathway. Mol. Med. Rep. 2015;11:3786–3793. doi: 10.3892/mmr.2015.3235. [DOI] [PubMed] [Google Scholar]
  • 61.Zhou M., Wang K., Jin Y., et al. Explore novel molecular mechanisms of FNDC5 in ischemia-reperfusion (I/R) injury by analyzing transcriptome changes in mouse model of skeletal muscle I/R injury with FNDC5 knockout. Cell. Signal. 2023:110959. doi: 10.1016/j.cellsig.2023.110959. [DOI] [PubMed] [Google Scholar]
  • 62.Romero-Becerra R., Santamans A.M., Folgueira C., Sabio G. p38 MAPK pathway in the heart: new insights in Health and disease. Int. J. Mol. Sci. 2020;21 doi: 10.3390/ijms21197412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Zhu N., Cai C., Zhou A., et al. Schisandrin B prevents hind limb from ischemia-reperfusion-induced oxidative stress and inflammation via MAPK/NF-kappaB pathways in rats. BioMed Res. Int. 2017;2017:4237973. doi: 10.1155/2017/4237973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Yang J.C., Lin M.W., Rau C.S., et al. Altered exosomal protein expression in the serum of NF-kappaB knockout mice following skeletal muscle ischemia-reperfusion injury. J. Biomed. Sci. 2015;22:40. doi: 10.1186/s12929-015-0147-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Park J.W., Qi W.N., Cai Y., Urbaniak J.R., Chen L.E. Proteasome inhibitor attenuates skeletal muscle reperfusion injury by blocking the pathway of nuclear factor-kappaB activation. Plast. Reconstr. Surg. 2007;120:1808–1818. doi: 10.1097/01.prs.0000287245.17319.57. [DOI] [PubMed] [Google Scholar]
  • 66.Lille S.T., Lefler S.R., Mowlavi A., et al. Inhibition of the initial wave of NF-kappaB activity in rat muscle reduces ischemia/reperfusion injury. Muscle Nerve. 2001;24:534–541. doi: 10.1002/mus.1037. [DOI] [PubMed] [Google Scholar]
  • 67.Cheng Y., Di S., Fan C., et al. SIRT1 activation by pterostilbene attenuates the skeletal muscle oxidative stress injury and mitochondrial dysfunction induced by ischemia reperfusion injury. Apoptosis. 2016;21:905–916. doi: 10.1007/s10495-016-1258-x. [DOI] [PubMed] [Google Scholar]
  • 68.Kuroda Y., Togashi H., Uchida T., et al. Oxidative stress evaluation of skeletal muscle in ischemia-reperfusion injury using enhanced magnetic resonance imaging. Sci. Rep. 2020;10:10863. doi: 10.1038/s41598-020-67336-4. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

mmc1.zip (10.2MB, zip)
mmc2.pdf (193.3KB, pdf)
mmc3.docx (443.7KB, docx)

Data Availability Statement

The datasets generated and/or analysed during the current study are available in the [The Science Citation Index Expanded of Clarivate Analytics’S Web of Science Core Collection (WoSCC)] repository, https://www.webofscience.com/wos/alldb/basic-search. We have uploaded the search results in Appendix 1 of the supplementary materials.

Articles from Heliyon are provided here courtesy of Elsevier

RESOURCES