Global research characteristics and trends of infection after spinal implant surgery: a bibliometric analysis

Introduction

Spinal fixation is the most successful and prominent technique used for spinal fractures, tumors, and deformities (1). As the number of spinal implant surgeries increases, the relative frequency of postoperative complications is also rising (2,3). Over the last few years, infections related to orthopedic devices have generated much attention (4-7). Infection is one of the most challenging complications following spinal implant surgery and is also associated with higher postoperative mortality, a longer length of stay, and higher hospital costs (8,9). Therefore, to further improve strategies in response to infection after spinal implant surgery (IASIS), a comprehensive and systematic approach to investigating the knowledge surrounding IASIS is required. Bibliometric analysis is an essential tool that applies statistical and mathematical approaches to explore the study characteristics and subject trends in a specific field (10-15). In recent years, several bibliometric studies of spinal disorders, such as cervical spondylotic myelopathy and spinal cord injury, have been conducted (16,17). To the best of our knowledge, the global status and research trends of IASIS have not yet been explored. Accordingly, the objectives of this study are to identify the global research characteristics and trends of IASIS from academic papers using a bibliometric approach.

Methods

Data source and search strategy

Literature was retrieved using Web of Science (data last updated on June 6, 2021) with the following search terms: spinal implant infection, infection associated with spinal implants, infection after instrumented spinal surgery, infection with spinal instrumentation, spine, spinal implant, instrumentation, instrumented, fusion, infection, and surgical site infection.

Two investigators (Cheng Li and Haiyang Wu) read the article titles and abstracts independently. Research articles were included if they (I) reported on research describing instrumented spine surgery with postoperative infection, (II) reported on basic research in spinal implant-associated infection, and (III) were published from January 1, 2000 to December 31, 2020. Articles were excluded if they contained research reporting infection in the absence of spinal implant surgery and/or were an article type that included conference proceedings, book chapters, retracted papers, editorials, errata, or letters.

Statistical analysis

Total records from the Web of Science were exported to plain text and Microsoft Excel (Microsoft, Redmond, WA, USA). WPS Office (Kingsoft, Beijing, China), VOSviewer (Leiden University, Leiden, the Netherlands), CiteSpace v. 5.7 R2 (Drexel University, Philadelphia, PA, USA), and Bibliometrix (University of Naples Federico II, Naples, Italy) software were used for analysis. Information analyzed included author, country, research direction, research trend, digital object identifier, journal title, institution, journal impact factor (2020), abstract, keywords, article title, language, and publication year. Research directions were defined into 5 groups: incidence, prevention, risk factor, diagnosis, and treatment. In the list of the top 5 most contributive authors, if several authors belong to the same institution, the author with the most publications was selected.. As a useful bibliometric indicator, the h-index was also included to assess scholarly productivity in IASIS (18).

Results

The specific literature screening steps are shown in Figure 1. A total of 820 publications on IASIS published over the last two decades were identified using the electronic Web of Science database. Of these, 805 papers were written in English, followed by German [7], French [4], and Spanish [2]. The remaining 2 publications were in Czech and Portuguese. The sum of times cited was 22,714 (16,851 without self-citations). The average number of citations per document was 27.7. The h-index of all articles related to IASIS was 74.

Figure 1 The specific literature screening steps.

Number of publications per year

Figure 2A outlines the specific number of annual publications related to IASIS. A model-fitting curve revealed a significant exponential growth trend in the past two decades (R²=0.9448). After 2012, the number of articles exceeded 40 per year. The year 2018 ranked as the most productive year [96], followed by 2019 and 2020 [88 and 86, respectively].

Figure 2 The distribution of publications and countries. (A) The specific number of annual publications on the topic of IASIS. (B) A world map depicting the contribution of each country in terms of publication counts. (C) The annual publication counts of the top 10 countries from 2000 to 2020. (D) The international cooperation analysis among different countries. The thickness of the line between 2 countries reflects the strength of the cooperation; the thicker the line, the stronger the cooperation. IASIS, infection after spinal implant surgery. IASIS, infection after spinal implant surgery.

Contributions of countries

A total of 46 countries published research on IASIS, including 24 European countries, 13 Asian countries, 4 South American countries, 2 North American countries, 2 African countries, and 1 Oceanian country (Figure 2B). The most prolific country was the United States, with the highest total citation count, average article citations, and h-index. Japan ranked second (77 articles), followed by China (73 articles; Table 1). The annual number of publications from the top 10 countries between 2000 and 2020 is illustrated in Figure 2C. The United States was consistently the major contributor in this field, and the number of publications from Asian countries, such as Japan and China, gradually increased from 2010. Figure 2D displays the international cooperation analysis among different countries. Researchers from the United States collaborated the most closely with those from Canada, Germany, and Japan.

Analysis of prolific institutions

Table 2 shows that the top 5 institutions contributing to the highest number of papers on IASIS were from the United States. The most productive organization was Johns Hopkins University (54 articles), followed by the University of California (49 articles) and the University of Virginia (30 articles). Regarding total citations, the University of California ranked first (1,914 citations), followed by Johns Hopkins University (1,840 citations) and Thomas Jefferson University (1,403 citations). With an h-index of 22, Johns Hopkins University was at the top of the ranking list, with the University of California second (h-index 21) and Thomas Jefferson University third (h-index 18). Figure 3A shows the network map of institution coauthorship analysis as conducted using VOSviewer. Publications originating from 31 institutions were selected, with a minimum number of 10 documents for each institution. The University of Virginia, the University of California San Francisco, and Johns Hopkins University were located centrally on the network map. Moreover, different nodes representing institutions were assigned distinct colors according to the average appearing year (AAY) based on the color gradient in the lower right corner. These institutions, including the Washington University, the University of Maryland, and Twin Cities Spine Center, are depicted in blue with smaller AAY values, indicating that most participants were potential early contributors to IASIS research. Correspondingly, Brown University, Columbia University, and Yale University were potential new entrants in this domain.

Figure 3 The distribution of institutions and authors. (A) Network map of institution coauthorship analysis. (B) The average outputs of the top 8 authors between 2000 and 2020. (C) Cluster density visualization map of author coauthorship analysis. (D) Network visualization map of author cocitation analysis.

Analysis of influential authors

A total of 3,569 authors contributed to this field. The author with the highest number of publications was Alexander R. Vaccaro (18 publications), followed by Justin S Smith (14 publications) and Amit Jain (12 publications). Alexander R. Vaccaro and Justin S Smith had the highest h-index (Table 3). Figure 3B depicts the average outputs of the top 8 authors between 2000 and 2019. A cluster density visualization map of the author coauthorship analysis is shown in Figure 3C. Authors with close associations were assigned to a cluster with the same color. Only authors with more than 5 publications were included, forming a total of 11 author clusters. As for author cocitation analysis, 100 authors with at least 30 citations were included in the analysis. The author with the most citations was Margaret A Olsen, followed by AFP ter Gunne and Albert F. Pull (Figure 3D).

Analysis of active journals

After reviewing the journal names, we ascertained that the Journal of Spinal Disorders & Techniques changed its name to Clinical Spine Surgery. This was also observed for the Journal of Bone and Joint Surgery, which changed its name to The Bone & Joint Journal. Hence, information on the respective journals was combined. In total, 145 different journals were found to contribute to this field.

Table 4 shows the top 10 journals with the most published articles. The journal with the highest number of publications and highest h-index was Spine (189 and 56, respectively), followed by European Spine Journal (62 and 22, respectively) and Spine Journal (47 and 20, respectively). According to the 2021 Thomson Reuters journal impact factor report, 136 journals had an impact factor for 2020. Approximately 25.7% (n=35) of the journals were ranked in the first quartile, 25% (n=34) were in the second quartile, 25% (n=34) were in the third quartile, and 24.3% (n=33) were in the fourth quartile. The top 10 journals with the most publications came from the first, second, and third quartiles (Table 5). The journal with the highest impact factor was Biomaterials (impact factor 12.479), followed by Advanced Healthcare Materials (impact factor 9.933) and European Journal of Nuclear Medicine and Molecular Imaging (impact factor 9.236). All of the top 10 highest impact factor journals were in the first quartile. Figure 4A depicts the year of each journal’s first paper on IASIS, with most journals appearing in 2016, 2017, and 2020 (14).

Figure 4 The distribution of journals. (A) Year of each journal’s first publication. (B) Network visualization map of the journal cocitation analysis. (C) A dual-map overlay of the journals on IASIS administration research. IASIS, infection after spinal implant surgery.

Figure 4B is the cocitation network visualization map of journals created by VOSviewer. Only journals with a minimum of 30 citations were visualized. The map contains 83 nodes, 3,174 links, and 6 clusters. The top 5 journals with the most citations were Spine, Journal of Bone and Joint Surgery-American Volume, European Spine Journal, Spine Journal, and Journal of Neurosurgery-Spine. Additionally, a dual-map overlay of the journals on IASIS research was also created (Figure 4C), which clarifies the citation patterns and knowledge flows in a given area. Four core citation paths are marked in pink on this map. It can be further observed that papers published in medicine, medical, or clinical journals cited journals mainly in the fields of molecular biology, genetics, health, nursing, medicine, psychology, education, and social science.

Research direction and trends

Regarding research type, 41 articles focused on basic research, whereas the remaining 779 publications were human studies. Among these 820 studies, 788 research directions were identified through article titles and abstracts. A single research topic was found in 770 papers, whereas 2 research subjects were identified in 18 articles. Most studies focused on the risk factors and the incidence of IASIS (Figure 5A). The changing pattern of the annual appearance frequency of author keywords, including risk factors, management, outcomes, prevention, and mortality, from 2000 to 2020 is illustrated in Figure 5B. Risk factors of IASIS were always a frequent focus in this field.

Figure 5 The distribution of the main research direction and author keywords. (A) Research directions of IASIS. (B) The changing pattern of annual appearance frequency in author keywords from 2000 to 2020. IASIS, infection after spinal implant surgery.

VOSviewer was used to explore research trends. Of the 1,496 keywords, the minimum number of occurrences of a keyword was set to 4. Figure 6 is the co-occurrence overlay visualization of 158 items; the closer the color is to red, the closer the research topic is to the present.

Figure 6 Analysis of the co-occurrence of keywords between 2000 and 2020.

The thematic map was established using Bibliometrix software, which outlined the internal relationships in different groups. Cluster 1 comprised the topics of diagnosis and treatment of IASIS, and the top 3 most frequent keywords were infection, spine, and surgery. Cluster 2 was associated with scoliosis-related infection, and the most used keywords were scoliosis, spinal deformity, and neuromuscular scoliosis. Cluster 3 was associated with risk factors and prevention of IASIS, and the most commonly occurring keywords were surgical site infection, spine surgery, and risk factors (Table 6).

Discussion

We conducted a bibliometric analysis to attain a comprehensive overview of the development and trends of scientific publications in the IASIS field over two decades and further analyzed relationships among citations and alternative indicators.

Number of publications per year

From 2000 to 2020, 820 IASIS-related studies were identified in this bibliometric study, with the annual global publication showing a substantial rise from 2012. This result may suggest that IASIS has generated increasing attention and interest over recent years.

Countries, institutions, and authors

Countries from Europe, Asia, and North America accounted for the top 10 contributing nations for IASIS research. The United States had the highest number of publications and academic impact worldwide. In addition to the IASIS research subject, earlier bibliometric analyses revealed that the United States also had the greatest number of publications in other areas of spinal research (19-21).

All the top 5 contributing authors and organizations were from the United States. Furthermore, US experts and institutions dominated the area of IASIS. Alexander R. Vaccaro from Thomas Jefferson University had the most publications and was one of the authors engaged in developing the consensus about infections of implants after spine surgery (6). The list of the top 5 contributing authors showed all authors to be surgeons, whereas a previous bibliometric study of periprosthetic joint infection (PJI) demonstrated microbiologists and infectious disease specialists to be key members in the management of IASIS (22). This finding likely reflects a current lack of multidisciplinary teams in IASIS management, and the creation of such teams could be helpful (23-25). The top 8 authors’ annual publications between 2000 to 2020 showed a higher yearly output and better continuity in the second decade than in the first decade. This finding may suggest that authors have increased their attention and concern for IASIS in the last decade.

Journals

Of the 145 journals, Spine had the highest number of relevant publications and the greatest academic influence on IASIS. Of the 136 journals with an impact factor, Biomaterials had the highest impact factor. According to data on the year in which journals published their first article, there was an increasing number of new journals interested in IASIS research.

Research direction and trends

Analysis of the research directions for the topic of IASIS showed that risk factors and incidence were most commonly investigated, whereas diagnosis-related research was least frequently researched. Due to the current lack of credible diagnostics for IASIS (26-29), further exploration is required. Keyword co-occurrence maps showed that the latest trends in IASIS research were likely linked to surgical site infection management and international consensus meeting (6,30-33).

Three research groups were identified in the cluster analysis. Cluster 1 encompassed the topic of diagnosis and treatment of IASIS. The C-reactive protein (CRP) blood test was highlighted in group 1, and it is also commonly used as a first-line diagnostic method for other orthopedic implant–associated infections, such as PJI and fracture-related infection (34-36). However, for low-virulence microorganisms, there was a high occurrence of CRP in the normal range (37,38). Thus, novel serum biomarkers are continually being explored (39-41). Sonication was the only microbiological diagnostic method present in cluster 1. One retrospective study (42) reported the diagnostic value of 2 intraoperative methods—tissue culture and sonication—for spinal implant infection. Implant sonication had a higher sensitivity and specificity than did tissue culture. Prinz et al. (43) reported the frequent detection of low-virulence bacteria via pedicle screw sonication. Cluster 1 contained the microbial-related words of Staphylococcus aureus and Staphylococcus epidermidis. An epidemiological study from 2000 to 2012 observed the most frequently isolated bacterial pathogens to be Staphylococcus epidermidis, followed by methicillin-sensitive Staphylococcus aureus, Cutibacterium acnes, and Escherichia coli (44). IASIS is commonly caused by Staphylococcus spp; therefore, the relationship between IASIS and Staphylococcus spp warrants further attention in clinical diagnosis. In terms of treatment, combined surgical debridement with antibiotic therapy is the major strategy for IASIS management (45,46). Additional studies also supported vacuum-assisted closure as a viable method for IASIS treatment (47-49).

Cluster 2 was associated with scoliosis-related infection. A study of 108,419 operations following spine surgery reported a higher postoperative infection rate in scoliosis surgery than in surgery for degenerative diseases, spondylolisthesis, and fractures (50). Therefore, infection prophylaxis and postoperative follow-up for patients with scoliosis require special attention. Neuromuscular and adolescent idiopathic scoliosis were identified in cluster 2, likely reflecting a difference in the incidence of infection among various scoliosis etiologies. A multicenter, retrospective study of surgical site infection among pediatric patients following scoliosis surgery found that patients with neuromuscular scoliosis had the highest infection rate (9.2%), followed by those with syndromic scoliosis (8.8%), other scoliosis types (8.4%), congenital scoliosis (3.9%), and idiopathic scoliosis (2.6%) (44). Cutibacterium acnes is a pathogen frequently found in infections following scoliosis surgery, especially in delayed infections (51-53). Cluster 3 was associated with risk factors and prevention of IASIS. The main concerns of IASIS in cluster 3 appeared to focus on obesity, body mass index, urinary tract infection, diabetes, albumin, malnutrition, smoking, and rheumatoid arthritis (54-61). Vancomycin powder is the most relevant research topic in IASIS prevention, and the efficacy of local vancomycin powder in decreasing the infection rate after spine surgery has become a research hotspot involving considerable controversy (62,63).

Conclusions

The number of publications on IASIS showed an increasing trend from 2000 to 2020. The United States was the most productive country and was home to the top authors and institutes. The most relevant and academically influential journal on IASIS was Spine. Risk factors and the incidence of IASIS were of interest to academics and clinicians, whereas diagnosis-related issues were overlooked. The most recent research trend is likely related to the management of IASIS and consensus on the topic.

Acknowledgments

We would like to thank Dr. Sundrela Kamhieh-Milz for editorial assistance.

Funding: The study was funded by the German Research Foundation (DFG) and the Open Access Publication Fund of Charité—Universitätsmedizin Berlin, Beijing Postdoctoral Research Foundation (No. 2022-ZZ-040), China Postdoctoral Science Foundation (No. 2022M720385).

Footnote

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://atm.amegroups.com/article/view/10.21037/atm-21-5044/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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