How far has diabetes‐related foot disease research progressed in Australia? A bibliometric review (1970–2023)

Abstract Background Diabetes‐related foot disease (DFD) is a leading cause of the Australian and global disease burdens and requires proportionate volumes of research to address. Bibliometric analyses are rigorous methods for exploring total research publications in a field to help identify volume trends, gaps and emerging areas of need. This bibliometric review aimed to explore the volume, authors, institutions, journals, collaborating countries, research types and funding sources of Australian publications investigating DFD over 50 years. Methods A systematic search of the Scopus® database was conducted by two independent authors to identify all Australian DFD literature published between 1970 and 2023. Bibliometric meta‐data were extracted from Scopus®, analyzed in Biblioshiny, an R Statistical Software interface, and publication volumes, authors, institutions, journals and collaborative countries were described. Publications were also categorised for research type and funding source. Results Overall, 332 eligible publications were included. Publication volume increased steadily over time, with largest volumes (78%) and a 7‐fold increase over the last decade. Mean co‐authors per publication was 5.6, mean journal impact factor was 2.9 and median citation was 9 (IQR2‐24). Most frequent authors were Peter Lazzarini (14%), Vivienne Chuter (8%) and Jonathon Golledge (7%). Most frequent institutions affiliated were Queensland University Technology (33%), University Sydney (30%) and James Cook University (25%). Most frequent journals published in were Journal Foot and Ankle Research (17%), Diabetic Medicine (7%), Journal Diabetes and its Complications (4%) and International Wound Journal (4%). Most frequent collaborating countries were the United Kingdom (9%), the Netherlands (6%) and the United States (5%). Leading research types were etiology (38%), treatment evaluation (25%) and health services research (13%). Leading funding sources were no funding (60%), internal institution (16%) and industry/philanthropic/international (10%). Conclusions Australian DFD research increased steadily until more dramatic increases were seen over the past decade. Most research received no funding and mainly investigated etiology, existing treatments or health services. Australian DFD researchers appear to be very productive, particularly in recent times, despite minimal funding indicating their resilience. However, if the field is to continue to rapidly grow and address the very large national DFD burden, much more research funding is needed in Australia, especially targeting prevention and clinical trials of new treatments in DFD.


| BACKGROUND
Diabetes is the most rapidly growing leading cause of the global burden of disease, affecting an estimated 527 million people worldwide [1,2].
Diabetes-related foot disease (DFD) is the leading cause of global diabetes-related hospitalisations, amputations and burden of disease, affecting an estimated 20 million people worldwide with an additional 130 million at risk [3,4].DFD is defined as infection, ulceration or tissue destruction of the foot in a person with diabetes, underpinned by peripheral neuropathy and/or peripheral artery disease [5][6][7].
Australia has been reported to have higher DFD-related hospitalisation and amputation rates than similar countries [7][8][9].However, substantial variation exists between different geographical areas within Australia and also within indigenous populations [10][11][12].It is estimated that on any given day in Australia, 50,000 people have DFD, 1000 are in hospital due to DFD, 12 will undergo a DFD-related amputation and four people will die due to DFD [13,14].It is currently estimated that 1%-2% of healthcare expenditure in Australia and globally is related to DFD, yet research into DFD attracts less than 0.01% of competitive research funding [14][15][16][17].
This disparity highlights the lack of focus on this major health problem 17 and greater research contributions in DFD are required to address this large burden.
It is also important to understand the institutions, researchers, research type and level of funding that mostly produce research in a field, such as DFD [18][19][20][21].For example, it has been reported that there is a gross disparity in the level of research funding for DFD compared to other conditions with similar burdens [14,16].However, it is not clear how the research type and level of funding is distributed for DFD research in Australia.Understanding the research taking place in Australia and the means by which it receives funding is important to help Australian researchers and funders prioritise research for consumers, clinicians, funders and peak bodies.This, in turn, should improve the allocation of funds to the research prioritised at addressing existing gaps in the evidence base that targets reductions in the burden of disease for individuals with DFD and the nation.
Significant advances in the understanding of DFD have been made through the conduct of research internationally [22,23].
Recent international bibliometric analyses have demonstrated that the global volume of research in DFD is increasing [18][19][20][21].While Australia is in the top 10 countries for total DFD research volume in these global bibliometric analyses [18,20,23], the trends in terms of volume, authors, institutions, journals, collaborating countries, research types and funding sources that drive this research within Australia have not been reported.In addition, it is unclear whether the research produced by Australian researchers targets priority areas for DFD stakeholders (including people with DFD) [17], or are aligned with international recommendations [24].Therefore, the objective of this study was to conduct a bibliometric review that aimed to explore the volume, authors, institutions, journals, collaborating countries, research types and funding sources of Australian research publications investigating DFD over 50 years.

| METHOD
This was a bibliometric analysis of Australian publications investigating DFD between January 1970 and November 2023 using data from the Scopus ® database (Elsevier, Amsterdam, the Netherlands).
We chose the Scopus ® database for several reasons.Firstly, Scopus ® currently has the largest abstract and citation database for research literature [25].Secondly, it allows searching by publication, author or affiliation, with the ability to refine results by access type, source type, year, language, author, affiliation and funding sponsor.Thirdly, it has over 71.2 million records post 1969, includes a broader range of journals than PubMed and Web of Science and its citation analysis is faster and includes more publications than the citation analysis of Web of Science [26].

| Search strategy
The Scopus search strategy terms were developed based on previous bibliometric research on DFD and are presented in Table 1 [19].The search and retrieval process are shown in the PRISMA flow diagram (Figure 1).

| Study selection
The titles and abstracts of all identified publications were downloaded from the Scopus ® database and exported into the online  [6,24].This included diabetes-related peripheral neuropathy, Charcot neuroarthropathy, peripheral artery disease, ulceration, infection and/or amputation.Publications were excluded if they were case reports, commentaries, conference abstracts, research letters, guidelines or editorials.Any conflicts were discussed between two authors (PT and MC) until consensus was reached.
Additional publications were identified by backward snowballing checks of reference lists [27].

| Data extraction
Metadata of all included publications were extracted from Scopus and imported into Biblioshiny ® (based on R version 3.6.1,Bibliometrix package version 2.2.1;University of Naples Federico II, Naples, Italy, 2016) [28] for data extraction.The following bibliometric indicators were extracted from each publication: year of publication, journal name, journal impact factor (IF) (in year prior to publication, 2023 using the Web of Science Journal Citation Reports™ tool [Clarivate Analytics, Philadelphia, Pennsylvania, USA]), number of citations (determined by the Scopus ® database [Elsevier, Amsterdam, Netherlands]), author names, total authors per manuscript and institutional and country affiliation of each author.

| Data synthesis
To investigate the areas of research focus, publications were categorised according to the research type dimension of the United Kingdom Clinical Research Commission (UKCRC) Health Research Classification System by one author (BMP) [29].This widely used system allows the classification of all types of health-related research from basic to applied research [29].This system classifies types of research activities using 48 codes within eight overarching groups: (1) underpinning research; (2)

| Most frequent authors, institutions, journals and collaborating countries
There were a total of 1025 unique authors from the 332 publications for a mean of 5.6 co-authors per publication.Table 3 displays the most frequent authors of the publications were Peter Lazzarini (14%), Vivienne Chuter (8%), and Jonathon Golledge (7%).Table 4 displays the most frequent institutional affiliations were the Queensland University of Technology (QUT) (33%), University of Sydney (30%) and James Cook University (25%).In 324 of the included publications, an Australian institution was the primary  Figure 3 presents the five most common countries in which research collaboration occurred including the United Kingdom (9%), followed by the Netherlands (6%) and the United States of America (5%).

| Most cited publications
Table 6 presents the most highly cited publications, which were a Cochrane systematic review by Bergin and Wraight [31] (n = 151) and two original research papers by Delbridge et al. [32] (n = 144) and Tapp et al. [33] (n = 135).[20], and tripled from 2010 to 2020 [23], with the United States of America accounting for approximately one third of all publications [20] However, there was a seven-fold increase in our findings indicating an increased attention to the DFD field by researchers in Australia in particular.Other factors that may have also influenced the increase in output include the work and role of international and national research bodies advocating for DFD, such as the International Working Group for the Diabetic Foot (IWGDF) and the establishment of Diabetes Feet Australia.In other broad chronic health conditions such as gout and osteoarthritis, there have been similar upward trajectories in increasing output in recent times; however, a much greater overall volume of scholarly output was also seen in these other conditions compared to DFD research [34,35].

| Leading funding sources
Citation frequency is commonly used as a quality indicator of published research and a marker of research impact in bibliometric analysis [19][20][21]34].Factors that may influence citation frequency include perceived quality of the research publication, quality of journal, relevance to the field (scope), accessibility (open access vs. subscription) and time to be cited [36].The overall impact of Australian research in DFD has been ranked as 10th in the world [23], utilising total citations as an indicator of impact.Globally, the 50 most highly cited publications in DFD range from 231 to 1661 total citations [18], with the highest cited global publication a systematic review on prevention of DFU by Singh et al. [37].Fifteen of these leading 50 publications globally were review articles, which suggest that reviews may be considered to be a highly credible source of information to researchers in the field.It may also be related to the  access and provide publication in a timely manner [39].Diabetes Care could be considered a leading journal within the DFD field with an impact factor of 16.2, and was one of the highest 10 journals Australian authors published in with six publications (2%).This journal was similarly placed in the highest 10 publications in the global DFD bibliometric analysis with 125 total publications [23].
Very high impact journals generally seek to publish robust multicentre trials, which are more broadly applicable and determine causality.These are currently not widely undertaken in Australian DFD research due to a lack of funding.The Journal of Foot and Ankle Research appears to be more accessible and may also have a greater interest in publishing foot specific DFD research compared to broader diabetes journal with much larger scope.This particular metric will be of interest in future bibliometric analyses as the field matures, as it would be expected that the number of publications in high impact journals will increase.
A previous bibliometric publication reported the characteristics of DFD research according to health dimensions [23]

Funding category a n (%)
Nil reported 200 (60) Australian competitive grants 24 (7) Other public sector 17 (5) Industry/philanthropic/international 35 ( Japan [45].The NHMRC reported a decrease in the total funding pool attributed to diabetes-related research in recent times from $65 million in 2013, to $42 million in 2021, with similar decreases seen in other chronic conditions including cardiovascular disease and obesity [46].This decrease in funding is despite the increasing prevalence of diabetes and its associated complications in the Australian population [47], and despite a strategy to support Australian DFD research output published by Diabetes Feet Australia, which included recommendations for the establishment of national research priorities, development of a clinical trials network and proportional investment in DFD research [13].Success rates for NHMRC researcher support (fellowship) schemes and project grants have also been negatively impacted and were higher in 2013 than in 2021 [48].The current reported success rates are much lower than similar national schemes in the United Kingdom and the United States [49,50].Furthermore, it was highlighted that NHMRC funding does not completely align with societal burden of disease and some national health priorities are better funded than others.However, diabetes was reported to have a higher proportion of NHMRC funding compared to other priority health areas [51].It is currently unclear whether researchers in the field of DFD apply for competitive funding or what the specific success rates are.Overall, the low apparent funding rate not only underscores the resilience of Australian researchers in DFD to complete their research without significant funding, but is probably also contributing to the lack of more resource intensive clinical trials in this area.
Some limitations of the current study should be considered.
Research funding reporting may be under-reported and therefore may not adequately represent actual sources of funding.Peer reviewed publications that are not indexed in Scopus ® would not have appeared in our search and therefore would not have been included, so some publications may have been missed.Additionally, our search terms may not have captured all of the research conducted in the field.However, this was based on previous bibliometric publications in the field to reduce the likelihood of such an occurrence and improve our comparability to those studies [19,21].Our exclusion criteria included letters and short reports which may have excluded some Australian original research publications, which are published in high-impact journals and/or are highly cited [4,41,52].
The exclusion of guidelines also would have influenced the median citations of publications, as guidelines are commonly cited and some include Australian authors [6,53].Further, whilst we used two independent authors to perform the abstract and full text screening process, the categorisation of research and funding classification was completed by a single author, with only a random sample checked by a second author, which may have led to some inaccuracies.

2 of 13 -
JOURNAL OF FOOT AND ANKLE RESEARCH systematic review application Covidence © (Veritas Health Innovation, Melbourne, Australia).Titles, abstracts and full text review were independently screened by two authors (PT and MC).Publications were included if they were original articles or systematic reviews, conducted by an Australian Institution and in Australian population, had at least one author with an Australian affiliation and were published in English.Publications were included if the field of research was related to DFD

Figure 1 ,
Supporting Information S1).Figure2shows the schematic trend of Australian produced DFD publications increased steadily from the first identified publication in 1983 (Figure2) until 2012, and then increased exponentially with a five-fold increase in annual publications from 2012 to 2021, with the highest output in 2021 (15%) and a total of 266 (68%) of publications occurring in the past decade.The total publications had a total of 6075 citations, with a mean citation rate of 5.6 per publication (median: 9, IQR 2-24, range 0-151), including 47 (14%) that were not yet cited.The median journal impact factor of the journals in which the publications were published was 2.9 (IQR: 2.4-4.1, range 0.29-16.2).

4 of 13 -
JOURNAL OF FOOT AND ANKLE RESEARCH affiliation.Nine publications included one author with an Australian affiliation.Table 5 displays the most frequent journals in which publications were published, which were the Journal of Foot and Ankle Research (17%), Diabetic Medicine (7%), International Wound Journal and Journal of Diabetes and its Complications (both 4%).

Figure 4
Figure 4 shows the proportion of publications categorised with the UKCRC Health Research Classification System, according to the onedigit overarching code groups and the two-digit codes, respectively.The research category with most Australian DFD publications were etiology (38%), evaluation of treatments (25%), health services research (13%), detection, screening and diagnosis (12%), and management of disease and conditions (11%).Very few publications were related to prevention of diseases and conditions (<1.0%) and development of treatments and therapeutic interventions (<1%).The interrater reliability of research type categorisation was 0.91, indicating excellent agreement.

F I G U R E 2 of 13 -
Abbreviations: DFD, diabetes-related foot disease; IF, impact factor.

8 of 13 -
JOURNAL OF FOOT AND ANKLE RESEARCHthat Australian researchers are investigating aetiological factors associated with DFD.Some important discoveries have occurred as a result of such research, including identifying that younger-onset type 2 diabetes is an independent risk factor for poor healing and hospitalisation[40,41].However, these important discoveries are based on large prospective multi-centre cohort studies, which are more representative and powerful than single-centre retrospective data.It is recommended that more prospective multi-centre studies would be particularly beneficial and add to the national evidence base in DFD research.The evaluation of existing treatments was the second most common research category, with a focus on the evaluation of existing medical devices.People with DFD often interact with medical devices, which include footwear, offloading devices, vascular assessment equipment and wound dressings and interventions.Smaller publications investigating these types of existing and often well used medical devices can also be conducted relatively inexpensively in organised clinical settings.However, very few publications in this category implemented randomised controlled trials evaluating a new treatment or intervention.This also appears consistent with the funding data.Randomised controlled trials are very resource intensive, and in Australia are funded primarily through the federal government's nationally competitive category one programmes.Similarly, low numbers of randomised controlled trials have been previously described in other DFD bibliometric analyses [9, 21], which also suggests that there are challenges in executing randomised controlled trials in this area of research.There has been very little Australian research in DFD prevention with only one percent of total publications focused on prevention.A recent bibliometric analysis of New Zealand-based DFD publications showed a greater local research focus on screening and prevention (30%) compared with Australia (<1%) [19].It is currently not possible to draw any further comparisons with other countries as the research categories have not been evaluated.The low numbers of publications F I G U R E 4 Research type for DFD Australian DFD publications categorized by the UKCRC Health Research Classification System.DFD, diabetes-related foot disease.T A B L E 7 Funding sources of Australian DFD publications.
Whilst the volume of scholarly work of Australian DFD researchers has dramatically increased in the last decade, there remains very small amounts of nationally competitive funding attributed to the field.Thus, many Australian DFD researchers are conducting research with little to no funding, and research outputs are based on feasible and pragmatic studies which are not necessarily being driven by need or priorities.Whilst this suggests that Australian DFD researchers are resilient and able to produce high volumes of output despite a lack of funding, there is a level of risk to the future viability of the field without substantial new competitive funding.In particular, future research should consider greater focus on prevention studies and the development and trials of new treatments, as the volume of local research in this area was substantially lacking.

Table 2
presents the publication characteristics of a total of 332 Australian publications related to DFD that were deemed eligible and

Table 7
shows the proportion of publications categorised by the Australian Government's categories of research funding received.Most publications reported no research funding (60%), with only University.Etiology was the most frequently published research type, followed by treatment evaluation and health services research.The majority of research did not report any funding sources.The substantial increase in Australian DFD research over the past 10 years is consistent with the DFD research reported internationally and in other nations, including New Zealand and Gulf countries [19-21, 23].Previous global DFD bibliometric analyses have demonstrated that publications have more than doubled worldwide from 2007 to 2017 Top 10 cited Australian DFD publications.
existing patients, treatments and services is likely comparatively less resource intensive than researching on much larger populations need for prevention studies and new treatments in trials.These existing types of research are not without challenges, however, and requires resources to create databases, validate tools and train clinicians, however does lend itself to in kind contributions.It is commendableT A B L E 6