Bone生长因子t形态形成蛋白(bmp)hat are members of the transforming growth factor–beta superfamily. BMPs are implicated in numerous physiological processes including bone formation and repair through stimulating osteoblast activity and further inducing the differentiation of mesenchymal progenitors into osteoblasts.1Clinically, previous studies have shown success using BMPs as an alternative for autograft in spinal fusion of various animal models.2- - - - - -6In humans, recombinant human BMP (rhBMP) is used in a variety of spine procedures including posterolateral lumbar spine fusion,7- - - - - -9posterior lumbar interbody fusion,10anterior lumbar interbody fusion,10- - - - - -12and anterior cervical discectomy and fusion (ACDF).13- - - - - -15Compared with iliac crest autograft, many studies favor the use of BMP to achieve higher rates of fusion and lower instances of nonunion,8,16,17along with decreasing blood loss and operative time.17,18相反,有些人没有发现区别the two methods of spinal fusion.9Despite the potential benefits of increased fusion rates, BMP usage also carries the risk of certain adverse events, which have been reported in later studies examining BMP.13,16,19,20
Overall, there remains some disagreement in the literature concerning the benefit in using BMP in spinal fusions. Furthermore, controversy exists regarding the complications implicated in BMP use that have more recently been published within the literature.14,21,22Given the extent of variability regarding reported BMP outcomes, it is imperative for clinicians to have a complete assessment of the literature. In this study, we performed a bibliometric analysis on the 100 most cited articles discussing BMP usage in spinal fusion to provide a thorough evaluation of the current literature. In addition, we provide a brief synopsis of specific topics examined and the types of articles present within the gathered literature.
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Search Strategy
Our search strategy was designed to capture all relevant published and indexed articles referring to bone morphogenetic proteins (BMPs) and spine surgery. We performed an extensive electronic search of Elsevier’s Scopus database in January 2022, which has a robust infrastructure to allow for citation analysis. Search dates were from 1955 to 2021. Scopus’s robust electronic abstract and citation database has indexed articles and documents from more than 41,000 journals, covers more than 12,000 publishers, and all included journals undergo a thorough review process to ensure a high quality of research.23The database was searched using Boolean criteria with keywords including "bone morphogenetic proteins" and "spine" in the title, abstract, and keywords. Our inclusion criteria for document selection required all documents to 1) describe clinical or basic science relevance to BMP and its application to spine surgery, and 2) involve BMP to a significant degree in the study. All discrepancies were resolved by discussion and consensus among authors.
Data Extraction
一个discrete set of validated bibliometric parameters was extracted: article title, year, authors, first and senior author names, Scopus citations, citation count, country/region and institution of the senior author, source and document type, affiliations, author and index keywords, and references. Other parameters that were assessed included the total number of articles and common bibliometric parameters such as localh-index, collaboration index, and average citations per article.
Statistical and Bibliometric Analyses
一个ll statistical and bibliometric analyses were performed using R version 4.1.2 (The R Foundation for Statistical Computing) using thebibliometrixpackage.24Various plots were created using theggplotpackage (Tidyverse,https://ggplot2.tidyverse.org/). A p value < 0.05 was considered significant.
Results
Search Results, Characteristics, and Citations
The search strategy yielded 6041 articles. The articles were sorted by decreasing citation counts and analyzed to determine emerging trends from all the publications pertaining to BMPs.Table 1outlines the characteristics of the search result, andTable 2lists the 10 most cited articles. In addition to citation count, we included citation rate per year, the primary investigator, the country/region of the primary investigator, and the journal in which the article was published, along with theh-index for a more thorough overview of these publications. The majority of identified publications were non-review articles (n = 63%); however, 30 reviews (30%), 5 conference papers (5%), and 2 short surveys (2%) were identified in our results. The average citation per publication for the 100 most cited articles was 279, while the average citation per year per publication was 18.
Summary of characteristics of the entire literature search
| Description | Results |
|---|---|
| Overall data | |
| Time span | 1994–2018 |
| Sources (e.g., journals, books) | 40 |
| Documents | 100 |
| Average yrs from publication | 17 |
| Average citations per document | 279 |
| Average citations per yr per publication | 17.69 |
| References | 6041 |
| Publication types | |
| Article | 63 |
| Conference paper | 5 |
| Review | 30 |
| Short survey | 2 |
| Keywords | |
| Indexed keywords | 1267 |
| Author’s keywords | 253 |
| 一个uthor information | |
| No. of authors | 391 |
| Author appearances | 472 |
| Authors of single-authored documents | 5 |
| multiauthored文档的作者 | 386 |
| Collaboration information | |
| Single-authored documents | 5 |
| Documents per author | 0.256 |
| Authors per document | 3.91 |
| Coauthors per documents | 4.72 |
| Collaboration index | 4.06 |
The 10 most cited articles about BMPs
| Rank | No. of Citations | Citation Rate/yr | 一个uthors & Year | Title | 开云手机版app下载安装最新版 | Country/Region |
|---|---|---|---|---|---|---|
| 1 | 1624 | 85.5 | Chen et al., 200427 | "Bone morphogenetic proteins" | Growth Factors | US |
| 2 | 1021 | 78.5 | Carragee et al., 201121 | "A critical review of recombinant human bone morphogenetic protein-2 trials in spinal surgery: emerging safety concerns and lessons learned" | Spine Journal | US |
| 3 | 780 | 39 | Cheng et al., 20031 | "Osteogenic activity of the fourteen types of human bone morphogenetic proteins (BMPs)" | Journal of Bone and Joint Surgery | US |
| 4 | 774 | 36.9 | Lieberman et al., 20025 | "The role of growth factors in the repair of bone. Biology and clinical applications" | Journal of Bone and Joint Surgery | US |
| 5 | 580 | 96.7 | Wang & Yeung, 201726 | "Bone grafts and biomaterials substitutes for bone defect repair: a review" | Bioactive Materials | Hong Kong |
| 6 | 575 | 27.4 | Boden et al., 20027 | "Use of recombinant human bone morphogenetic protein-2 to achieve posterolateral lumbar spine fusion in humans: a prospective, randomized clinical pilot trial: 2002 Volvo Award in clinical studies" | Spine | US |
| 7 | 567 | 28.4 | Geiger et al., 20036 | "Collagen sponges for bone regeneration with rhBMP-2" | 一个dvanced Drug Delivery Reviews | US |
| 8 | 548 | 23.8 | Boden et al., 200025 | "The use of rhBMP-2 in interbody fusion cages. Definitive evidence of osteoinduction in humans: a preliminary report" | Spine | US |
| 9 | 541 | 31.8 | Shields et al., 200613 | "Adverse effects associated with high-dose recombinant human bone morphogenetic protein-2 use in anterior cervical spine fusion" | Spine | US |
| 10 | 501 | 23.9 | Burkus et al., 200211 | "Anterior lumbar interbody fusion using rhBMP-2 with tapered interbody cages" | Journal of Spinal Disorders & Techniques | US |
Within the 10 most cited articles, there was an even split of basic science and clinical articles, with 5 articles focused on each discipline. Six studies were reviews, 3 were clinical trials, and 1 was a retrospective chart review. Of the 3 clinical trials, 2 received industry funding to conduct their study.7,25The majority of the top 10 studies were published prior to 2010 (n = 8; 80%), and only 2 were published following 2010 (20%). All articles in the top 10 were conducted in the United States except for the study by Wang et al. in Hong Kong.26
一个mong the 10 most cited articles, the median citation count was 577 (range 501–1624). The most cited article to date, "Bone morphogenetic proteins," is a basic science article published in 2004 by Chen et al.27It has been cited 1624 times in the literature. This review eloquently summarizes the physiological function of BMPs and outlines the compound’s current and potential clinical uses. Alternatively, "Bone grafts and biomaterials substitutes for bone defect repair: a review" had the highest citation rate with 96.7 citations each year.26The article was authored by Wang et al. in 2017.Similar to the paper by Chen et al., this article provides a comprehensive review of BMPs and provides insight to new discoveries and clinical uses of it since the previous review was published.
Years of Publication
一个ll 100 most cited articles were published between 1994 to 2018 with bimodal peaks occurring at 2002 (n = 11 published articles) and 2007 (n = 10 published articles) (Fig. 1andTable 3). Only 3 articles (3%) were published after 2015. However, when analyzing the citation rate for each year between 1994 and 2018, the highest rates of citation occurred during 2016 and 2018 (citation rates of 68.667 and 68.75, respectively), thereby highlighting the continued interest in BMPs.
一个nnual number of papers produced by year from 1994 to 2018. Figure is available in color online only.
Comparison of the 100 most cited BMP articles in spine surgery by article type
| Variable | Basic Science Articles, n = 33 | Clinical Articles, n = 67 | p Value |
|---|---|---|---|
| Citations, median (range) | 157 (119–780) | 190 (116–1021) | 0.222 |
| Citations/yr, median (range) | 11.3 (5.38–85.47) | 11.5 (4.31–96.67) | 0.866 |
| Yr of publication, median (range) | 2005 (1996–2015) | 2004 (1994–2018) | 0.719 |
| Country/region, n (%) | 0.140 | ||
| US | 27 (82) | 63 (94) | |
| Other | 6 (18) | 4 (6) | |
| Journal, n (%) | 0.188 | ||
| Spine | 12 (36) | 18 (27) | |
| Spine Journal | 1 (3) | 9 (13) | |
| JSDT* | 2 (6) | 4 (6) | |
| Other | 19 (55) | 36 (54) |
JSDT =Journal of Spinal Disorders & Techniques.
"Evaluation of human bone morphogenetic protein 2 in a canine spinal fusion model" by Muschler et al. was the earliest published article in our bibliometric analysis (1994).28However, we cannot discuss BMPs without acknowledging the work of Dr. Marshall Urist and his contribution to this field, given that he coined the term "bone morphogenetic proteins" and published his seminal paper "Bone morphogenetic protein" in 1971.29
一个uthors, Countries/Regions of Correspondence, and Affiliated Institutions
一个total of 391 authors contributed to these 100 most cited articles. The authors with the highest number of citations and published articles on the topic of BMP are listed inTable 4. Boden (Emory University) holds the highest total citation count with 2386 over 8 articles, Burkus (Columbus, Georgia) had the second highest citation count with 1913 over 7 articles, and Sandhu (Stanford University) had the third highest citation count with 1570.
The 10 most cited authors
| 一个uthor | No. of Articles | Total Citations |
|---|---|---|
| Boden SD | 8 | 2386 |
| Burkus JK | 7 | 1913 |
| Sandhu HS | 7 | 1570 |
| Toth JM | 5 | 964 |
| Glassman SD | 4 | 1157 |
| Lieberman JR | 4 | 1334 |
| Wozney JM | 4 | 1049 |
| Zdeblick TA | 4 | 1440 |
| Carragee EJ | 3 | 1350 |
| Carreon LY | 3 | 1350 |
| Einhorn TA | 3 | 1127 |
| Gornet MF | 3 | 964 |
| Heller JG | 3 | 1094 |
| Hurwitz EL | 3 | 1350 |
| Kanim LEA | 3 | 477 |
| Lane JM | 3 | 754 |
| Sethi A | 3 | 496 |
| Vaccaro AR | 3 | 602 |
| Vaidya R | 3 | 496 |
| 王JC | 3 | 517 |
一个uthors from 16 countries/regions have published highly cited works on BMP’s use in spinal surgery. The United States has the greatest number of citations (n = 23,761), followed by Hong Kong (n = 580), and the United Kingdom (n = 490) (Table 5). However, publications from Hong Kong, Portugal, and Australia had the highest average citations per article (n = 580, n = 421, and n = 323, respectively). For institutions, Emory University (United States) was the most represented affiliation of the top 100 publications (n = 14; 14%) (Table 6). Other highly represented institutions included the Hughston Clinic with 9 publications (9%), Hospital for Special Surgery with 6 (6%), and University of California with 6 (6%), all located in the United States.
The 10 countries with the most cited BMP articles
| Country/Region | Total Citations | 一个verage Article Citations |
|---|---|---|
| US | 23,761 | 290 |
| Hong Kong | 580 | 580 |
| United Kingdom | 490 | 245 |
| Georgia | 456 | 228 |
| Portugal | 421 | 421 |
| France | 416 | 208 |
| 一个ustralia | 323 | 323 |
| Sweden | 170 | 170 |
| Spain | 166 | 166 |
| Switzerland | 154 | 154 |
| Germany | 149 | 149 |
| Canada | 143 | 143 |
Top 10 affiliations
| 一个ffiliation | No. of Articles |
|---|---|
| Emory | 14 |
| Hughston Clinic | 9 |
| Hospital for Special Surgery | 6 |
| University of California | 6 |
| Medical College of Wisconsin | 5 |
| UCLA School of Medicine | 5 |
| Henry Ford Hospital | 4 |
| University of Virginia | 4 |
| University of Wisconsin | 4 |
| William Beaumont Hospital | 4 |
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The top 100 most cited articles were published in more than 12 journals overall (Fig. 2).Spinepublished the most articles discussing BMP with 29 publications (29%), followed bySpine Journalwith 10 publications (10%), andJournal of Spinal Disorders & Techniqueswith 7 publications (7%). Four articles (40%) within the 10 highest citation counts were published inSpine, most of which were basic science studies.
Most relevant sources/journals with 2 or more of the 100 most cited BMP publications. Figure is available in color online only.
Citation Comparisons
Within the topics of the included publications, 67 (67%) were clinically focused, and 33 (33%) were basic science focused. The citation counts and rates were compared between basic science and clinical studies (Table 3). The median citation count and rate were not statistically different between the two groups. The median years of publication for basic science and clinical articles were 2005 and 2004, respectively (p = 0.719). The United States was a common source for most of the publications regardless of the area of focus, accounting for 82% and 94% of all basic science and clinical articles, respectively, within this field (p = 0.14). Overall, there were no differences detected between basic science and clinical articles when comparing select bibliometric parameters.
Discussion
We completed a bibliometric analysis of the 100 most cited articles about BMP to evaluate the growth of the field over the years and to identify influential authors and institutions that have impacted this field. We found that many of the articles were published throughout the 2000s, while the number of citations increased in the years following 2010. Approximately two-thirds of articles were clinically focused, while the remainder were basic science–focused articles. Although most articles were published in the United States (mainly from Emory University), many authors worldwide have contributed to this continuously growing field.
In the initial discovery phase of BMPs, publications were mainly basic science in nature and focused on the role of BMPs in bone physiology. The seminal paper on BMPs was written and published by Urist and Strates.29Dr. Urist introduced his discovery of this protein to the scientific community and focused on understanding the role of BMPs in bone physiology and pathophysiology using in vitro models developed from rat cortical bones. While other authors have made impactful contributions to this field, the contributions of Dr. Urist cannot be understated. Following these principles established by Dr. Urist, for the next 30 years BMP basic science research aimed to investigate the efficacy of 1) BMPs in different in vivo animal models and 2) use in different areas of the skeleton to induce bone formation. Specifically, spinal fusion became an increased area of investigation during the 1990s. Studies by Schimandle et al.30and Sandhu et al.4demonstrated that BMPs could achieve lumbar intertransverse process fusions in rabbit and dog models, respectively, while Boden et al. showed the effectiveness of BMP as a bone graft substitute inside a titanium threaded interbody fusion cage in a rhesus monkey model for use during anterior spinal fusion.31By the late 1990s, the majority of BMP research was conducted in nonhuman primates.3,32,33
One of the first studies to explore the use of BMPs in humans was that by Boden et al., "The use of rhBMP-2 in interbody fusion cages. Definitive evidence of osteoinduction in humans: a preliminary report" (rank 8 in our bibliometric analysis).25Following this study, research productivity in this field significantly rose in 2002 (Fig. 1), with multiple groups investigating BMP use in lumbar spine surgery. From these studies, most investigations concluded that BMP use in lumbar fusion resulted in more favorable results (i.e., higher rates of fusion) compared with iliac crest autograft;7,11,34however, some found that there was no difference between the two methods.9By the mid-2000s, experiments began investigating BMP use beyond the lumbar spine to include ACDF.35,36
Despite these early studies showing somewhat overwhelming success for the use of BMPs in spinal fusion, literature published in the late 2000s and early 2010s began to highlight some longer-term complications that were not previously reported. Furthermore, controversy in the BMP field arose, with some studies suggesting that the rates of adverse events were underreported in the original clinical trials.14,21,22For instance, some studies suggested that BMP may be associated with an increased incidence of cancer, although this association is still under debate.16Other commonly reported adverse events include ectopic bone formation, excess bone resorption, and inflammation.16,19In addition, BMP usage in ACDF has been reported to have higher rates of complications,13,20with clinically significant swelling being a well-cited adverse event.14Currently, rhBMP-2 is approved by the FDA for bone repair including single-level spinal fusion due to degenerative disc disease between L2 and S5; however, use in the cervical spine was not approved by the FDA because of the described high rates of adverse events.
Regarding the future of BMP, principles discovered in the early basic science studies will continue to influence and guide research on BMP. However, we hypothesize that future publications will mostly consist of clinical studies that continue to examine various facets of BMP use in clinical practice, from potential complications to improved delivery techniques to increase its efficacy and likelihood of bone fusion. Currently, the vast majority of BMPs have been used off label, and therefore further analysis of the true outcomes would be helpful for this field. One additional area of concern in the current literature is the inherent conflicts that reside in industry-funded publications. For instance, of the 10 most cited studies, 2 of the 3 clinical trials received industry funding for completion of their studies. Therefore, we suggest that future studies conducted in this field should avoid, if possible, industry-funded research to stay impartial and present a truly objective report of the results without conflicts from the industry that could serve as potential confounders.
Limitations
引文的数量可以阻止的方法之一mining an article’s quality and/or its impact on the scientific community; however, determining a paper’s quality or impact requires more scrutiny than such generalized approaches. Papers that have been published earlier tend to have a higher number of citations than those that may have been recently published; in such cases, the number of citations per year may serve as a better measure of an article’s true popularity or impact. On the other hand, the accessibility to journals and sources of information is now greater than it has ever been. As such, more recent articles will have a larger accessible audience that may seemingly create the impression that it has a higher impact compared with an article that was published earlier. The number of citations is often correlated with the impact of an article on a given field; however, some of the most impactful ideas become widely accepted as common knowledge, and the original author may no longer be cited in future articles (this is a concept known as "obliteration by incorporation"). This phenomenon is observed with Dr. Urist’s seminal paper,29which, surprisingly, is not one of the most cited articles in the field.
Conclusions
BMPs were first introduced to the scientific literature by Dr. Urist in 1971.29Following the discovery of BMPs, there have been advances in our understanding of BMP physiology and its potential clinical use in spinal surgery. While early scientific efforts focused on basic science research on BMPs to advance our understanding of its mechanism of action in promoting bone formation, the majority of the more recent publications are clinically focused. Our analysis of the 100 most cited works in this field has highlighted the trends in the field and the progression from preclinical basic science research to the use of BMPs in clinical settings. Discovering the role of BMPs in bone formation and repair has had a major impact on the orthopedic field as a whole, especially spinal surgery. While BMPs have been used clinically for some time, there is a need for objective clinical trials and other high impact studies—preferably without industry funding—to establish noninferiority and superiority over autogenous bone grafts.
Disclosures
The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
一个uthor Contributions
Conception and design: Bydon, Shoushtari, Bauman. Acquisition of data: Shoushtari, Bauman, Durrani. Analysis and interpretation of data: Shoushtari, Bauman, Durrani, Nathani. Drafting the article: Shoushtari. Critically revising the article: Shoushtari, Bauman, Nathani. Reviewed submitted version of manuscript: Bydon, Shoushtari, Nathani. Approved the final version of the manuscript on behalf of all authors: Bydon. Statistical analysis: Shoushtari, Nathani. Administrative/technical/material support: Bydon. Study supervision: Bydon.
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