The 50 most influential papers pertaining to the Ilizarov method: A bibliometric analysis

The Ilizarov method has become a widely recognised surgical technique. A bibliometric analysis of the 50 most-cited publications relating to the Ilizarov method was carried out. Cumulative number of citations was 4,918. Mean number of citations was 98. h-index was 50. Impact factor of these journals ranged from 0.5-5.082. Our study suggests that a highly cited and influential paper likely originated from an American journal with a high impact factor and was published in the 1990s/2000s. Our compilation of the 50 most influential papers on the Ilizarov method will prove invaluable to those in training and those involved in further advancing the technique.


Introduction
Prof Gavriil Ilizarov's career began treating returning World War II soldiers. Famously, his method of distraction osteogenesis for bone lengthening was discovered by accident when callus was seen in a subject who distracted his frame instead of the usual compression. 1 Ilizarov's method made its first appearance in peer-reviewed journals almost 40 years ago. 2 The peak of its application, outside of its well-known usage in Russia, came during the 1990s. 3 As we will see in this study, the 1990s also coincided with the peak of published papers on its use. 3 As a testament to its success in bone repair and reconstruction, we have seen in the range of 50-100 articles on its various uses published each year. 4 It offers an alternative solution to bone conditions that may otherwise have been solved with more drastic measures such as amputation. [5][6][7] Despite the degree of expertise needed to perform correctly and its steep learning curve, it has gained popularity in many countries.
Our understanding of this technique has grown with its continued use and multiple publications. We stand to learn much from those that have gone before us with this technique and their experiences in the published literature are a crucial part of advancements in the field. An in-depth look and subsequent ranking of these publications allows us to ascertain which papers have had the most influence in terms of our clinical decision-making.
Citations are a form of recognition between authors of the impact that a colleague's work has had on their own research. Looking at how frequently an article is cited, we can evaluate the impact that article has had on the progression of the field in question. Citations are used in the metric for determining an article's impact factor (IF). We are drawn to journals with a higher impact factor and so citations can be said to indirectly influence the journals we read. IF is equal to the total number of citations for all publications in a journal over the past year divided by the total number of publications published in that journal in the previous two years. 8 Other authors have sought to find the most influential papers across a broad range of surgical specialties including orthopaedics, 9 plastics, 10 breast surgery, 11 general surgery 12 and urology. 13 Within the discipline of orthopaedics, there have been citation analyses published in the areas of hip and knee arthroplasty, 14 shoulder surgery, 15 spinal deformity surgery 16 and foot and ankle. 17 A bibliometric analysis of all articles containing the word "bone lengthening" was published in 2019. However, this paper dealt with other methods of bone lengthening, not solely the Ilizarov method. It also only included papers published from 2001 to 2017. 18 To our knowledge, this is the first study examining the most influential papers relating to the Ilizarov method.
Our aim with this study was to discover the 50 most-cited papers pertaining to the Ilizarov method by carrying out a bibliometric analysis of previous publications using the Web of Science database (see Fig. 1).

Methods
To examine the top 50 articles regarding the Ilizarov method, the Web of Science Collection search engine was employed in August 2021. A single search term, "Ilizarov method" was used and articles from 1945 to 2021 were examined. There were no limitations applied to our search filter. 1,480 papers were recovered on the initial search. These papers were then ordered from most citations to least number of citations. Two independent authors reviewed the results and complete agreement between authors was required for an article to be included. If an abstract did not yield sufficient information to decide on article inclusion, a fulltext review was carried out. Papers deemed not relevant to the Ilizarov method were excluded. The first 75 papers were examined thoroughly. This led to the exclusion of 25 papers based on irrelevance to the topic in question (Fig. 2). A decision was made to conclude our search at 75 papers as after that, the number of citations per paper did not fall dramatically. To illustrate this point, the difference in citations between the 75th and the 100th paper was 7. The remaining 50 most-cited papers were put into tables. Further analysis of these papers was carried out based on various factors: mean citation number, the year of publication, publishing institution, country of origin and what journal it was published in. Publication year was divided into decades. The calculation for mean citation number involved dividing the number of citations an article has by the number of years that had passed since it was published.

Results
The cumulative total of citations for the most-cited 50 publications was 4,918. Each paper was cited 98 times on average. The h-index of this list of articles was 50. The top 50 articles can be found in Table 1. The most-cited paper was by Gavriil Ilizarov himself with 428 citations, published in 1988. 19 The 50th paper was by Birch 20 and was cited 52 times. The oldest paper was published in 1988, again this was Ilizarov's above-mentioned paper "The principles of the Ilizarov method". 19 The most recent publication came from Papakostidis et al. 21 in the Bone and Joint Journal in 2013, who performed a systematic review of the Ilizarov method in patients with long bone defects.
The 1990s saw the greatest number of papers (n = 27). The 20 year period between 1990 and 2010 made up 94% of the top 50 papers ( Table 2). These 50 papers were published in 20 unique journals. The impact factors of these journals ranged from 0.5 to 5.082. The language of publication in all instances was English. These publications represented several research areas including orthopaedics, general surgery, paediatrics, rheumatology, sport sciences and maxillofacial surgery.  Table 3. 10 unique countries contributed to the top 50. USA provided the most articles with 24 (48%), followed by Italy with 5 (10%) and Netherlands with 5 (10%). A full list of countries of origin can be found in Table 4. 10 different authors provided the top 50 articles. All authors publishing 2 or more papers can be found in Table 5. Paley appeared most frequently as first author with 6 (12%). This was closely followed by Lafeber and Von Roermund with 4 papers each (8%). Gavriil Ilizarov himself authored 2 papers (4%).

Discussion
In our study,we searched the Web of Science database to find the 50 most-cited papers on the Ilizarov method. In this way, we hoped to establish the papers which had influenced the field. A citation analysis such as this one, is important to the wider orthopaedic community as it chronicles the papers, authors, journals and eras that have shaped the discipline as we know it. Our study provides insight into the practicechanging developments that have taken place over the past 76 years.
In our study, citation number was used to estimate the influence of a certain paper and warrant its inclusion in the top 75. This method of citation analysis has been debated by some, 22 and does carry limitations which have been discussed by previous authors. 10 What it does allow for however, is a gauge of peer-recognition and allows us to examine the readership of an article. One must remember that number of citations does not directly correspond with study quality. For example, poorly-designed studies (by present day standards), may have a higher number of citations than a more recent study purely because it has had more time to accrue citations. If an article does have a high number of citations, it indicates that other researchers found its content useful. IF, a measure of citations, plays a vital role in how we interpret research and so these indicators are at the forefront of everyone's mind when critically analysing any piece of research.
The most-cited paper was "The principles of the Ilizarov method" 19 (1988) published by Ilizarov himself. This paper has been cited on 428 occasions. Its average citation number is 12.59. This article is based on a speech he delivered at the Annual Scientific Program of the Alumni association, supplemented by material he previously presented at a three-day international conference on the Ilizarov techniques for managing problematic skeletal issues.
The second most-cited paper was Paley's "Ilizarov bone transport treatment for tibial defects" 23 which was published in the Journal of Orthopaedic Trauma in 2000. His article was cited a total of 224 times with a mean citation number of 10.18. He conducted a retrospective case series of 19 patients with tibial defects treated with the Ilizarov method. All patients went on to achieve union. He found that his results compared favourably to other studies looking at other methods of bone grafting and even other studies concerning the Ilizarov method itself, particularly taking into account the size of the defect in his patients. While this paper has fewer citations in terms of absolute number than number one on our list, it is important to acknowledge that it was published 12 years later and its mean citation number (10.18) is quite respectable compared to 12.59 for the top-cited paper. Ilizarov's paper also dealt with the underlying principles of the technique and so would be relevant to a wider audience whereas Paley's only looked at the technique in the context of tibial defects. However, his contribution to the field of limb lengthening and reconstruction is evident as he was first author on the highest number (n = 6) of papers in this study (Table 5).
10 unique countries contributed to the top 50, with the USA contributing the majority (Table 4). That the USA contributed the highest number of papers should come as no surprise, as this has been reflected in other studies of a similar nature. 24,25 This finding also is in keeping with the high volume of orthopaedic clinical and academic activity exhibited by the USA. The 1990s and 2000s were the most prolific time periods with 94% (n = 47) of papers published in this era ( Table 2). 20 unique journals contributed to the top 50 (Table 3). An American journal, Clinical Orthopaedics & Related Research, had the highest number of publications with 13 (Table 3), again illustrating the influence that American studies have had on the field. Indeed, 4 out of the top 5 journals in terms of absolute publication number are American. Barring Ilizarov's paper at number 1, papers 1-5 on the list came from prestigious journals with IF in the range of 2.512-4.73. Our research would suggest that for a paper on the Ilizarov method to be highly-cited and influential, it likely originated from an American journal, with a high impact factor and was published in the 1990s/2000s.
There are several inherent limitations to a bibliometric analysis such as ours. This has been detailed and acknowledged by previous authors carrying out a similar study type. 16,26 The Web of Science Collection search engine extends from the present day as far back as 1945. For this reason, any articles published before then are automatically excluded and there is a real possibility of excluding some of the "classic" papers on the Ilizarov method. Previous citation analyses in other areas placed limits on their search. There were no restrictions on our search and the authors felt this reduced the possibility of excluding potentially relevant articles. It has been alluded to in previous studies that more recent papers (that may be of a potentially higher quality) are disadvantaged as the "classic" papers have been around for longer and thus have had greater opportunity for citation. Our use of the mean citation number is our attempt to control for this and to allow us to make a meaningful comparison between contemporary and historic papers.
Aspects of a bibliometric analysis make it difficult to control for bias, as was the case in our study. Self-citation, language bias, journal bias and in-house bias (among others) were not controlled for in this study. 27 There are several phenomena that can influence the results of a bibliometric analysis. Obliteration by incorporation is one of these. This refers to the highly-influential or "classic" articles becoming incorporated into clinical practice and widely-acknowledged and so, the need to cite them no longer remains. 28 Incomplete citing may also occur within papers if an author is attempting to persuade their audience instead of acknowledging a previous piece of work. 29

Conclusion
Our study highlights the 50 most-cited papers pertaining to the Ilizarov method. In this way, we have established those papers which have influenced the development and implementation of the technique. We have seen the journals, countries and authors that have made the greatest contribution. We are aware that a citation analysis does not directly measure scientific quality but it does indicate those papers   The effect of low-intensity pulsed ultrasound on callus maturation in tibial distraction osteogenesis which have significantly contributed to the area of interest. This compilation of influential papers will prove invaluable to orthopaedic trainees along with those involved in advancing the Ilizarov method as a surgical technique.

Funding
"This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors."

Declaration of competing interest
"The authors have no conflicts of interest to disclose."