Global Trends and Current Status in Osteonecrosis of the Femoral Head: A Bibliometric Analysis of Publications in the Last 30 Years

Zeqin Wen; Yusheng Li; Zijun Cai; Meng Fan; Jian Wang; Ran Ding; Cheng Huang; Wenfeng Xiao

doi:10.3389/fendo.2022.897439

. 2022 Jun 15;13:897439. doi: 10.3389/fendo.2022.897439

Global Trends and Current Status in Osteonecrosis of the Femoral Head: A Bibliometric Analysis of Publications in the Last 30 Years

Zeqin Wen ^1,^†, Yusheng Li ^1,^2,^†, Zijun Cai ^1,^†, Meng Fan ³, Jian Wang ³, Ran Ding ^3,^*, Cheng Huang ^3,^*, Wenfeng Xiao ^1,^2,^*

PMCID: PMC9240286 PMID: 35784575

Abstract

Introduction

Osteonecrosis of the femoral head (ONFH) is a progressive and disabling disease with severe socioeconomic burdens. In the last 30 years, a growing number of publications have reported significant advances in understanding ONFH. However, only a few studies have clarified its global trends and current status. Thus, the purpose of our study was to summarize the global trends and current status in ONFH through bibliometrics.

Materials and Methods

Publications related to ONFH from 1991 to 2020 were searched from the Web of Science (WOS) core collection database. The data were analyzed with bibliometric methods. Microsoft Excel was used for statistical analysis and to draw bar charts. SPSS was applied to perform linear regression analysis. VOSviewer was used to conduct bibliographic coupling analysis, co-authorship analysis, co-citation analysis and co-occurrence analysis.

Results

A total of 5,523 publications were covered. The United States consistently ranked first in total publications, sum of times cited, average citations per item and H-index. Kyushu University was the main contributor to ONFH. Clinical Orthopaedics and Related Research was the major publishing channels for ONFH-related articles. Takuaki Yamamoto published the most ONFH-related articles. Studies regarding ONFH could be divided into five clusters: 1) mechanism study, 2) treatment study, 3) complication study, 4) radiological study and 5) etiological study. Mechanism study might become a hot spot in the future.

Conclusions

The total number of publications in ONFH has generally increased over the last three decades. The United States was the leading country in ONFH research. Transplantation, engineering, cell and molecular biology, pharmacology and endocrinology have gradually increased and become hot topics in ONFH research. Mechanism study in ONFH including mesenchymal stem cells, apoptosis, oxidative stress, adipogenesis, osteogenic differentiation and endothelial progenitor cells, have attracted more attention and will become a hot spot in the future.

Keywords: osteonecrosis of the femoral head, bibliometric analysis, global trends, current status, the last 30 years

Introduction

Osteonecrosis of the femoral head (ONFH) is a disease in which local death of osteocytes and bone marrow components occurs due to venous stasis or impaired arterial blood supply or disruption of the femoral head (1). ONFH can be divided into two major types: traumatic and nontraumatic ONFH (1). Traumatic ONFH is mainly caused by femoral head and neck fracture, acetabular fracture, hip dislocation, and severe hip sprain or contusion (2–5). The main etiology for nontraumatic ONFH is long-term or excessive glucocorticoid (GC) administration, alcohol overconsumption, hemoglobin diseases and autoimmune diseases (1, 6, 7). However, the detailed pathogenesis of ONFH is not fully understood (8). Severe ONFH can lead to the collapse of subchondral bone and eventually damage to the hip joint, resulting in labor capacity losses for themselves and substantial economic losses for their families (9). It is estimated that 20,000 new cases of osteonecrosis are diagnosed in the United States each year, and the cumulative number of patients with ONFH ranges from 300,000 to 600,000 (10). Patients with advanced ONFH often do not respond well to medical treatment and require total hip arthroplasty (THA). However, THA, especially for young people, may lead to a series of complications, including dislocation, periprosthetic fracture, infection and prosthesis loosening (11). Therefore, the severe socioeconomic burdens and limited treatment options have forced us to continue to study the pathogenesis of ONFH and develop effective treatments for ONFH.

In the last 30 years, a growing number of publications have reported significant advances in the pathogenesis and treatment of ONFH worldwide. However, to the best of our knowledge, only a few studies have clarified the global trends and current status in ONFH. Bibliometrics is a method to cognize the global trends and current status of a certain field and evaluate the contributions of a collection of research results such as all publications of the same scholar, institution or country, by collecting the metrology characteristics of the publications (12–14). In addition, bibliometrics can also be used to guide policy formulation (15). Currently, bibliometric analysis has been used in a wide range of fields, including anesthesia, cancer, orthopedics and neurology, to compare the contributions of different research findings (13, 16–18). Therefore, the purpose of our study is to evaluate and summarize the global trends and current status in ONFH by analyzing ONFH-related publications in the last 30 years with bibliometrics to help researchers understand the research perspectives, hot spots and trends of ONFH.

Materials and Methods

Data Sources

The search was conducted using the Web of Science (WOS) Core Collection database, including Science Citation Index Expanded (SCI-Expanded), Social Sciences Citation Index (SSCI), Arts and Humanities Citation Index (A&HCI), Conference Proceedings Citation Index-Science (CPCI-S), Conference Proceedings Citation Index-Social Science and Humanities (CPCI-SSH), Book Citation Index-Science (BKCI-S), Book Citation Index-Social Science & Humanities (BKCI-SSH), Emerging Sources Citation Index (ESCI), Current Chemical Reactions Expanded (CCR-Expanded) and Index Chemicus (IC). The journal impact factors (IF) came from the 2020 version Journal Citation Reports except for Journal of Bone and Joint Surgery-British Volume from the 2014 edition and Proceedings of the Institution of Mechanical Engineers. Part H-Journal of Engineering in Medicine from 2002 edition.

Search Strategy

All the literature was retrieved in WOS on September 2, 2021. The search terms were TS = (osteonecrosis of femoral head OR necrosis of femoral head OR femoral head necrosis OR femoral head necrosis) AND LANGUAGE: (English) AND DOCUMENT TYPES: (Article OR Review). For the time span, we chose the 30 years between 1991 and 2020.

Data Collection

Full records and cited references were extracted from the retrieved literature for bibliometric analysis, such as titles, years of publications, authors, nationalities, institutions of authors, funding sources, journals of publications, abstracts, keywords, total number of publications, sum times of cited, average citations per item and H-index. The information based on bibliometric characteristics was downloaded from WOS and imported into Microsoft Excel 2017 and VOSviewer (v.1.6.17) for analysis.

Bibliometric Analysis

Microsoft Excel 2017 was used for statistical analysis and graphing of all the bar charts in the study. In addition, SPSS (v.26.0, IBM, New York, USA) was applied to perform linear regression analysis on the trends of total publications in the last 30 years. Any p values P < 0.05 were considered statistically significant. R ² represents the degree to which the linear regression model explains the overall variance (19).

VOSviewer is a software for plotting maps based on network data. In the network visualization, items are represented by circles. The size of the circle is determined by the number of publications of the item. The distance between two circles approximately indicates the relatedness of the items. The color of an item is determined by the cluster to which the item belongs. In this study, VOSviewer was used for conducting bibliographic coupling analysis, co-authorship analysis, co-citation analysis and co-occurrence analysis.

Results and Discussion

Global Trends of Publications in ONFH

A total of 5,523 ONFH-related literature published between 1991 and 2020 were identified in our study. The total publications of ONFH generally increased over time (R ² = 0.872, P < 0.001). The annual publications regarding ONFH have grown nearly sevenfold over the three decades from 61 in 1991 to 481 in 2020 ( Figure 1A ). A total of 98 countries/regions published ONFH-related literature, with the top twenty countries/regions shown in Figure 1B . Among them, the United States published the most literature (1,369, 24.787%), followed by China (1,246, 22.560%), Japan (544, 9.850%), Germany (303, 5.486%), England (283, 5.124%) and South Korea (281, 5.088%). The United States and China published more than twice as many articles as Japan. Moreover, the total number of ONFH publications in each country or region also increased over time: the United States (R ² = 0.732, P < 0.001), China (R ² = 0.661, P < 0.001), Japan (R ² = 0.525, P < 0.001), Germany (R ² = 0.755, P < 0.001), England (R ² = 0.679, P < 0.001) and South Korea (R ² = 0.805, P < 0.001) ( Figure 1C ). Figure 1D shows the number of publications from individual countries or regions visually in the heatmap.

Global trends of publications on osteonecrosis of the femoral head (ONFH) in the last 30 years. **(A)** Annual ONFH-related publications worldwide. **(B)** The total number and percentage of ONFH-related publications from the top twenty countries/regions. **(C)** ONFH-related publications of the top six countries/regions over time. **(D)** Heatmap displaying the distribution of ONFH-related publications globally.

Bibliometric analysis could be used to evaluate the current status and forecast future directions (20). Therefore, our study was conducted to evaluate and summarize the global trends and current status of ONFH in the last 30 years. As demonstrated in this study, the number of ONFH-related publications has increased significantly over the past three decades from 1991 to 2020. We could predict that ONFH-related publications would continue to increase over time in the coming years. It was easy to conclude from the heatmap that researchers from all over the world were involved in ONFH research, particularly in North America, East Asia and Europe. Highly developed economies and the prevalence of ONFH in these regions may explain this result. China’s contribution was lower than that of the United States before 2013 and gradually surpassed the United States after 2013, even though the total number of publications of the United States in the last 30 years was still more than that of China. This reasonable explanation might be attributed to the rapid national development and the corresponding annually increased research funding for ONFH.

Quality Analysis of Global Publications

Country

Figure 2A illustrates the sum of times cited, average citations per item and H-index of the top ten countries with the most publications associated with ONFH. Among the top ten countries, the sum of times cited (45,314), average citations per item (33.1) and H-index (94) of the United States, the first-ranked country regarding total publications, were all higher than those of the other nine countries. In terms of the total publications, China ranked second. However, China ranked ninth in average citations per item (11.33), just above India. Other developed countries, including Japan, Germany, England, South Korea, France, Canada and Italy, all had relatively high average citations per item and H-index despite the small number of publications.

Quality analysis of global publications in ONFH in the last 30 years. **(A)** Total publications, sum of times cited, average citations per item, and H-index of the top ten countries by contributions. **(B)** Total publications, sum of times cited, average citations per item, and H-index of the top ten institutions by contributions. **(C)** Total publications, sum of times cited, average citations per item, and H-index of the top ten authors by contributions.

In terms of total publications, the sum of times cited, average citations per item and H-index, the United States ranked first in the world and is the leading country in ONFH. China was in second place by the number of total publications and the sum of times cited, ranking third in the H-index, while it only surpassed India in average citations per item among the top ten countries. This means that while China held a leading position in the contributions of ONFH, there was still a significant gap between China and developed countries with regard to the academic level of ONFH research. This situation may be caused by the scientific evaluation system of China favoring the number rather than the quality of publications in the past.

Institution

Over the past three decades, approximately 3,721 institutions worldwide have published ONFH-related literature. Figure 2B details the top ten most contributing institutions all over the world. Of the ten institutions, five were in China (Shanghai Jiao Tong University, Dalian University, Guangzhou University of Chinese Medicine, Huazhong University of Science and Technology and Xi’an Jiaotong University), two were in Japan (Kyushu University and Osaka University), two were in the United States (Hospital for Special Surgery and Duke University) and one was in South Korea (Seoul National University). The institution making the greatest contribution to ONFH research is Kyushu University, with 115 publications, 2,675 citations, 23.26 average citations and an H-index of 27. Shanghai Jiao Tong University came in second place (107 publications, 1,676 citations, 15.66 average citations and H-index of 20), followed by Osaka University (74 publications, 1,982 citations, 26.78 average citations and H-index of 27), Seoul National University (66 publications, 1,381 citations, 20.92 average citations and H-index of 22) and Dalian University (61 publications, 992 citations, 16.26 average citations and H-index of 16). Interestingly, the top ten most contributing institutions were all from the top ten countries, indicating that the establishment of outstanding institutions was the prerequisite to improve the academic level of a country.

Author

Analyzing the quality of publications by the author, the top ten contributors to ONFH are presented in Figure 2C . Of the ten authors, five were from Japan (Takuaki Yamamoto, Yukihide Iwamoto, Goro Motomura, Nobuhiko Sugano and Yasuharu Nakashima), two were from China (Dewei Zhao and Changqing Zhang), two were from the United States (Michael A. Mont and Harry K. W. Kim) and the remaining author was from South Korea (Kyung-Hoi Koo). Moreover, eight of these authors were from the top ten institutions: four were from Kyushu University (Takuaki Yamamoto, Yukihide Iwamoto, Goro Motomura and Yasuharu Nakashima), Nobuhiko Sugano was from Osaka University, Dewei Zhao was from Dalian University, Changqing Zhang was from Shanghai Jiao Tong University and Kyung-Hoi Koo was from Seoul National University. The greatest contributor was Takuaki Yamamoto, with 94 publications, 2,379 citations, 25.31 average citations and an H-index of 29. Michael A. Mont, who ranked second in publications, had the greatest number of citations, average citations and highest H-index among the top ten authors (79 publications, 4,927 citations, 62.37 average citations and H-index of 36).

In other words, the top ten authors who contributed most to ONFH were also from the top ten countries and eight of them worked for the top ten institutions. This interesting finding suggested a win–win situation between excellent scientific platforms and first-class scholars. The excellent scientific platforms provided sufficient scientific funds and advanced experimental equipment for top scholars, who were likely to make great contributions to the advancement of such platforms.

Quality Analysis of Journal and Funding Agency

Journal

The top ten journals publishing the most ONFH-related literature are shown in Figure 3A . Clinical Orthopaedics and Related Research (IF = 4.291, 2020) was the most active journal in ONFH research, with 348 articles, followed by International Orthopaedics (IF = 3.075, 2020), with 186 articles; Journal of Bone and Joint Surgery-American Volume (IF = 5.284, 2020), with 183 articles; Journal of Arthroplasty (IF = 4.757, 2020), with 154 articles; Journal of Pediatric Orthopaedics (IF = 2.324, 2020), with 132 articles; and Archives of Orthopaedic and Trauma Surgery (IF = 3.067, 2020), with 129 articles. From the top ten journals, we could track the latest advances in ONFH by monitoring the latest research of these journals.

Among the top ten journals, Clinical Orthopaedics and Related Research published the most ONFH-related articles, nearly twice as many as the publications of the second-ranked journal, International Orthopaedics. Additionally, Clinical Orthopaedics and Related Research (13,092 citations, 37.62 average citations and H-index of 58) had the most total citations, although the average citations per item were relatively low among the top ten journals. In contrast, the third-ranked journal, Journal of Bone and Joint Surgery-American Volume, had the highest average citations and H-index (13,072 citations, 76.9 average citations and H-index of 71). In addition, Journal of Bone and Joint Surgery-British Volume had relatively high average citations per item and H-index (8,602 citations, 70.51 average citations and H-index of 51). The higher average citations per item and H-index to some extent indicated the high quality of their publications.

Funding Agency

Figure 3B presents the top ten funding agencies with the most ONFH-related articles. Globally, the National Natural Science Foundation of China (NSFC, China) funded the most articles with the maximum number of citations (528 publications, 6,739 citations, 12.69 average citations and H-index of 37). The United States Department of Health Human Services (HHS, the United States) ranked second (168 publications, 6,712 citations, 39.95 average citations and H-index of 43), followed by the National Institutes of Health (NIH, the United States) (165 publications, 6,338 citations, 38.41 average citations and H-index of 43), Ministry of Education Culture Sports Science and Technology (MEXT, Japan) (99 publications, 1,216 citations, 11.92 average citations and H-index of 19), Japan Society for the Promotion of Science (JSPS, Japan) (92 publications, 1,156 citations, 12.17 average citations and H-index of 18) and National Institute of Arthritis Musculoskeletal Skin Diseases (NIAMS, the United States) (72 publications, 2,613 citations, 36.29 average citations and H-index of 28). Thanks to the substantial funding from NSFC, China ranked second in terms of the number of ONFH-related publications.

Top Ten Most Cited Publications in ONFH

Table 1 shows the top ten most cited publications in ONFH. The top ten publications were published from 1992 to 2012 and the number of citations ranged from 372 to 892. The second, fourth and seventh most cited publications were written by Mont et al., Mankin, and Assouline-Dayan et al. (22, 24, 27). They all comprehensively summarized the etiology, pathogenesis, pathology, diagnosis and treatment of ONFH. Moreover, the ninth most cited publication was written by Steinberg et al., which introduced the Steinberg classification system for ONFH diagnosis, staging and treatment (29). Other literature in the top ten most cited publications involved other topics related to ONFH, such as hip surgery, fracture and trauma. In addition, the vast majority of the top ten most cited publications were published before 2010 and only one article was published in 2012, which was to be expected, as recently published articles take time to be widely cited.

Table 1.

Top ten most cited publications in osteonecrosis of femoral head (ONFH) in the world.

Title	Author	Journal	Year	Type	IF	Times cited
Surgical dislocation of the adult hip - A technique with full access to the femoral head and acetabulum without the risk of avascular necrosis	Ganz, R et al. (21)	Journal of Bone and Joint Surgery-British Volume	2001	Article	3.309	892
Non-traumatic avascular necrosis of the femoral head	Mont, MA and Hungerford (22),	Journal of Bone and Joint Surgery-American Volume	1995	Review	5.284	746
Fractures of the acetabulum: Accuracy of reduction and clinical results in patients managed operatively within three weeks after the injury	Matta, JM (23)	Journal of Bone and Joint Surgery-American Volume	1996	Article	5.284	733
Nontraumatic necrosis of bone (osteonecrosis)	Mankin, HJ (24)	New England Journal of Medicine	1992	Review	91.253	600
Anterior femoroacetabular impingement Part II. Midterm results of surgical treatment	Beck, M et al. (25)	Clinical Orthopaedics and Related Research	2004	Article	4.291	511
Biological reactions to wear debris in total joint replacement	Ingham, E et al. (26)	Proceedings of the Institution of Mechanical Engineers. Part H-Journal of Engineering in Medicine	2000	Review	0.740	491
Pathogenesis and natural history of osteonecrosis	Assouline-Dayan, Y et al. (27)	Seminars in Arthritis and Rheumatism	2002	Review	5.532	475
Anatomy of the medial femoral circumflex artery and its surgical implications	Gautier, E et al. (28)	Journal of Bone and Joint Surgery-British Volume	2000	Article	3.309	436
A quantitative system for staging avascular necrosis	Steinberg, ME et al. (29)	Journal of Bone and Joint Surgery-British Volume	1995	Article	3.309	435
Corrosion at the head-neck taper as a cause for adverse local tissue reactions after total hip arthroplasty	Cooper, HJ et al. (30)	Journal of Bone and Joint Surgery-American Volume	2012	Article	5.284	372

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Research Areas Analysis

The ONFH-related articles published from 1991 to 2020 were categorized into 83 different research areas on WOS. However, to more intuitively show the changes in the research areas over time, we merged the areas of similar significance and finally selected 12 research areas. Figure 4A presents all the research areas and the corresponding number of ONFH-related articles, among which the orthopaedics area received the most attention (1,568, 28.390%), followed by surgery (945, 17.110%), medical imaging (567, 10.266%), transplantation (534, 9.669%), engineering (402, 7.279%), cell and molecular biology (390, 7.061%), pharmacology (271, 4.907%), endocrinology (264, 4.780%), pathology (240, 4.345%), pediatrics (139, 2.571%), oncology (111, 2.010%) and rheumatology (92, 1.666%). Figure 4B shows the distribution of ONFH-related research areas during 1991-2000, 2001-2010 and 2011-2020, from which we could obviously find the changes in ONFH-related research areas. Orthopaedics, surgery and medical imaging have always been the research areas of greatest concern, even though the popularity of medical imaging has decreased to some extent. Over time, research in transplantation, engineering, cell and molecular biology, pharmacology, and endocrinology has increased considerably. Pathology, pediatrics, oncology and rheumatology have not received much attention all the time.

Research area analysis of global publications in ONFH in the last 30 years. **(A)** Research areas in ONFH. **(B)** Radar map of research areas in ONFH during 1991-2000, 2001-2010 and 2011-2020.

Orthopaedics, surgery and medical imaging have been extensively and intensively studied due to their focus on the risk factors, etiology, diagnosis and treatment of ONFH. With the development of vascularized bone grafts, bone marrow mesenchymal stem cell transplantation and endothelial progenitor cell transplantation, an increasing number of studies have been conducted to test the efficacy and safety of transplant therapy for ONFH through animal experiments or clinical trials. Furthermore, researchers combined transplantation with cell and molecular biology to enhance the efficacy of transplant therapy for ONFH. For example, Hang et al. evaluated the efficacy of vascular endothelial growth factor 165 (VEGF165) transgenic bone marrow mesenchymal stem cells in mongrel dogs with ONFH (31). In the engineering area, novel biomechanical analysis, materials and implants related to ONFH are hotspots in this field. For example, Wang et al. developed a device referred to as the super-elastic cage for the treatment of Ficat and Arlet stage II and III ONFH (32). In addition to surgical treatment, researchers explored drug therapy, which we classified into pharmacology. In recent years, some traditional Chinese medicines have gradually been studied for ONFH treatment, such as Panax notoginseng saponin, bone-strengthening pills and Huogu I formula (33–35). Endocrinology focused on the effects and mechanisms of long-term or excessive GC administration on ONFH. Pediatrics, oncology and rheumatology mainly studied the role of Legg-Calvé-Perthes disease, leukemia and systemic lupus erythematosus in the pathogenesis of ONFH, respectively. Legg-Calvé-Perthes disease is the most prevailing juvenile form of idiopathic ONFH, affecting children 2-14 years old (36). ONFH is one of the most common and debilitating therapy-related side effects of antileukemic treatment and is associated with the treatment of GCs, asparaginase (ASP) and methotrexate (MTX), genetic factors and age (37). Similarly, ONFH is also one of the serious and well-recognized complications of SLE and the use of GCs, an impaired immune microenvironment and the complex pathogenesis of SLE are synergistically involved in the pathogenesis of ONFH (38).

Bibliographic Coupling Analysis

Bibliographic coupling analysis is a method exhibiting the relatedness of items based on the number of references they share, which is established when two items cited the same article. Bibliographic coupling analysis was used in this study to establish the similarity relationship among publications from the three dimensions of country, institution and journal. To some extent, the total link strength of a particular item can explain its worldwide influence. Items with higher total link strength indicate that the countries/institutions/authors are more globally influential.