1Canterbury District Health Board, Christchurch Hospital, Christchurch, New Zealand; 2Directorate General of Planning & Studies, Ministry of Health, Muscat, Oman; 3Edgar Diabetes & Obesity Research Centre, Dunedin School of Medicine, University of Otago, Dunedin, New Zealand *Corresponding Author’s e-mail: ibra.3sk@gmail.com أحباث مرض القدم السكري يف دول جملس التعاون اخلليجي حتليل ببليوغرايف اإبراهيم �شالح البو�شعيدي، نادية نور عبد الهادي، كري�شنت كوبيل abstract: Objectives: Countries in the Gulf Cooperation Council (GCC) have some of the highest prevalence rates of diabetes mellitus (DM) in the world; however, DM-related research activity in this region is limited. This study aimed to examine trends in published diabetic foot disease (DFD) research undertaken in GCC countries. Methods: This bibliometric study was conducted in December 2016. Standardised criteria were used to search the MEDLINE® database (National Library of Medicine, Bethesda, Maryland, USA) for DFD-related publications authored by GCC researchers between January 1990 and December 2015. Various details such as the type of publication, journal impact factor and number of article citations were analysed. Results: A total of 96 research articles were identified. The number of publications per year significantly increased from nil prior to 1991 to 15 in 2015 (P <0.01). Basic/clinical research articles accounted for 96.9% of publications, with three randomised controlled trials and no systematic reviews/meta-analyses. When adjusted for population size, Kuwait had the highest number of published papers per year, followed by Bahrain and Qatar. The number of authors per publication significantly increased during the study period (P = 0.02). However, 16 articles (16.7%) had no citations. The median journal impact factor was 0.15 ± 1.19 (range: 0–6.04). Conclusion: The number of publications authored by GCC researchers has risen in recent years. Increasing research funding and promoting collaboration between local and international researchers and institutes are recommended to bolster research regarding DFD prevention and management in GCC countries. Keywords: Bibliometric Analysis; Diabetes Mellitus; Diabetic Foot; Research; Publications; Arab Countries; Gulf Cooperation Council. فاإن ذلك، ومع العامل. دول ببقية مقارنة عاليا اخلليجي التعاون جمل�ص دول يف ال�شكري مر�ص انت�شار معدل يعترب الهدف: امللخ�ص: القدم مر�ص جمال يف املن�شورة الأبحاث حتليل اإىل الدرا�شة هذه تهدف حمدودة. املنطقة هذه يف بال�شكري املتعلقة البحثية الأن�شطة ال�شكري يف دول جمل�ص التعاون اخلليجي. الطريقة: مت اإجراء هذه الدرا�شة الببليوغرافية يف دي�شمرب 2016. با�شتخدام معايري بحثيه موحدة املقالت جميع لتحديد الأمريكية( املتحدة الوليات ماريالند، بيثي�شدا، للطب، الوطنية )املكتبة ميدلين البيانات قاعدة يف البحث مت املتعلقة مبر�ص القدم ال�شكري التي ن�رسها باحثني من دول جمل�ص التعاون اخلليجي بني يناير 1990 ودي�شمرب 2015. مت جمع وحتليل عدد من البيانات من �شمنها نوع املن�شورة الطبية، عامل تاأثري املجلة، ومعدل القتبا�ص. النتائج: مت حتديد ما جمموعه 96 بحثا من�شورا. مت مالحظة ازدياد عدد املن�شورات ب�شكل كبري من ل �شيء يف �شنة 1991 اإىل 15 يف �شنة P >0.01( 2015(. �شكلت البحوث املخربية/ال�رسيرية %96.9 من اإجمايل املن�شورات فيما كان هناك ثالثة جتارب ع�شوائية حمكومة وعدم وجود اأي مراجعات منهجية/حتاليل تلوية. كانت الكويت اأكرث الدول من حيث عدد املن�شورات الطبية عند مقارنتها مع حجم ال�شكان، تليها البحرين وقطر. لقد لوحظ ازدياد عدد املوؤلفني لكل من�شور مع الوقت خالل فرتة الدرا�شة )P = 0.02(. ومع ذلك، كان 16 )%16.7( بحثا من�شورا بدون اقتبا�ص. كان متو�شط عامل تاأثري املجلة 1.19 ± 0.15 )جمال: 6.04-0(. اخلال�صة: لقد زادت عدد املن�شورات يف دول جمل�ص التعاون اخلليجي على مدى ال�شنوات املا�شية. دعم الأن�شطة البحثية املتعلقة بعالج والوقاية من مر�ص القدم ال�شكري يف دول جمل�ص التعاون اخلليجي يتطلب زيادة متويل البحوث الطبية وت�شجيع التعاون بني الباحثني ومراكز البحوث داخليا وخارجيا. الكلمات املفتاحية: حتليل ببليوغرايف؛ ال�شكري؛ القدم ال�شكري؛ بحث؛ من�شورات؛ الدول العربية؛ جمل�ص التعاون اخلليجي. Diabetic Foot Disease Research in Gulf Cooperation Council Countries A bibliometric analysis *Ibrahim S. Al-Busaidi,1 Nadia N. Abdulhadi,2 Kirsten J. Coppell3 clinical & basic research Sultan Qaboos University Med J, August 2018, Vol. 18, Iss. 3, pp. e338–343, Epub. 19 Dec 18 Submitted 20 Dec 17 Revision Req. 6 Feb 18; Revision Recd. 6 Mar 18 Accepted 29 Mar 18 Advances in Knowledge - This study presents a systematic bibliometric analysis of diabetic foot disease (DFD) research originating from the Gulf Cooperation Council (GCC) region. - Although the number of DFD-related publications showed a slow but significant increase between 1990 and 2015, GCC countries still lag behind other countries in this field, despite having some of the highest diabetes mellitus (DM) prevalence rates worldwide. Application to Patient Care - The findings of this study are intended to highlight and promote research related to the epidemiology, management and prevention of DFD in GCC countries. Such research efforts would help to inform patient care, policy planning and DM management in this region. doi: 10.18295/squmj.2018.18.03.012 Ibrahim S. Al-Busaidi, Nadia N. Abdulhadi and Kirsten J. Coppell Clinical and Basic Research | e339 Diabetes mellitus (dm) is a public health challenge in the Arabian Gulf region.1 With an estimated population of 53 million, the Gulf Cooperation Council (GCC) consists of the member states of Bahrain, Kuwait, Oman, Qatar, Saudi Arabia and the United Arab Emirates (UAE), all of which share similar demographic characteristics, socioeconomic profiles and healthcare systems.2 Over the past five decades, these countries have undergone rapid economic growth and urbanisation, facilitating lifestyle changes which have contributed to a marked rise in the prevalence of obesity and nutrition-related noncommunicable diseases, such as type 2 DM.3 Overall, GCC countries have some of the highest global age-adjusted DM prevalence rates among adults, ranging from 14.8% in Oman to 20% in Kuwait, Qatar and Saudi Arabia.1 Moreover, the health- care systems of GCC countries are inadequately resourced and structured to tackle the growing DM burden, resulting in suboptimal care.4,5 Poorly-controlled DM increases the risk of compl- ications such as diabetic foot disease (DFD), a group of heterogeneous conditions which cause deformity, ulcer- ation and infection due to peripheral neuropathy and vascular disease in the lower limbs.6 Worldwide, DFD is associated with significant morbidity and mortality, in addition to being a major financial burden to both individuals and healthcare systems.7,8 The lifetime risk of an individual with DM developing a foot ulcer is approximately 25%.8 Foot ulceration increases the risk of lower limb amputation, one of the most debilitating complications of DM. More than 50% of non-traumatic lower limb amputations are attributable to DFD.8 Population-based studies conducted in high-income countries have shown the prevalence of active diabetic foot ulcers to be 1–5%, which is much lower than rates reported in certain middle- and low-income countries (>11%).7,8 Marked differences have also been observed in GCC countries, with the prevalence of diabetic foot ulcers ranging from 0.2% in the UAE to 5.9% in Bahrain.9 While DM-related lower limb amputations are reportedly uncommon (1.1%) among patients attending primary care centres in Saudi Arabia, 47.3% of all lower limb amputations in Oman are performed on DM patients.10,11 Current understanding of DFD has become possible as a result of decades of international research and collab- oration.7 Nevertheless, locally driven DM-related research, particularly regarding DFD, appears to be limited in the GCC region, despite the high DM prevalence rates.5,11,12 Publication in peer-reviewed journals is generally reg- arded as one of the key indicators of research product- ivity.13,14 In a recent bibliometric analysis, Alzahrani et al. examined the research contributions of 22 Arab countries to the DFD literature and found that only 11.6% of 906 DM publications were related to DFD, although the highest number of publications originated from GCC countries.15 However, this study had methodological limitations. Only articles published between January 1996 and April 2012 were examined; in addition, non- original research studies were included.15 Moreover, publication-related characteristics (e.g. the quality of the publications and extent of local and international collab- oration) were not evaluated. The aim of the current study was to provide an updated analysis of DFD-related publications emanating from GCC countries and to examine trends in public- ation quality and quantity. Specifically, the study aimed to determine the total number and type of GCC- produced DFD-related publications, country-specific contributions, the degree of local and international research collaboration and the impact of the publ- ished research. Methods This study was conducted in December 2016 and inv- olved a bibliometric analysis of DFD-related public- ations authored or co-authored by researchers from the GCC region. A comprehensive literature search for relev- ant publications was conducted using the MEDLINE® database (National Library of Medicine, Bethesda, Mary- land, USA), the largest and most widely used biomedical indexing database in the world.16 Two search strategies were employed—the first using Medical Subject Headings (MeSH) classifications and the second based on free- text searching—to ensure maximal retrieval of relevant articles. In both strategies, the following search terms were used in combination with the Boolean operator “or”: “diabetes”, “diabetes complications”, “diabetic foot”, “diabetic foot disease”, “diabetic foot ulcer”, “peripheral arterial disease”, “peripheral neuropathy”, “diabetic foot ulceration” and “amputation”. The Boolean operator “and” was then used to link these terms to the ethnogeograph- ical terms “Gulf Cooperation Council”, “GCC”, “Arabian Gulf”, “Arab”, “Arabs”, “Bahrain”, “Kuwait”, “Oman”, “Qatar”, “Saudi Arabia” and “United Arab Emirates”. The reference lists of identified articles, as well as any Scopus® citations (Elsevier, Amsterdam, the Netherlands), were also scanned to find additional publications. Subsequently, the titles and abstracts of identified publications were reviewed. For an article to be incl- uded in the study, the research had to have been cond- ucted in one or more of the GCC countries and the author(s) based in the GCC region (i.e. affiliated with a GCC medical or research centre). Furthermore, only English-language articles related to DFD and its comp- onents (e.g. DM-related peripheral neuropathy, periph- eral vascular disease, infections, deformity, ulceration and/or amputation) published between January 1990 Diabetic Foot Disease Research in Gulf Cooperation Council Countries A bibliometric analysis e340 | SQU Medical Journal, August 2018, Volume 18, Issue 3 and December 2015 were included in the study. Non- original research publications, including reviews, case reports, commentaries, letters and editorials, were excl- uded from the study. Thereafter, the remaining public- ations were classified into three general categories—basic/ clinical research papers, systematic reviews/meta analyses and randomised controlled trials (RCTs)—based on their level of evidence as defined by the Oxford Centre for Evidence-based Medicine.17 For each included publication, various author- and article-related data were extracted, including the number of authors, their institutional affiliations, the year and type of publication and the name of the publishing journal at the time of publication. In addition, the degree of local (defined as the presence of authors affiliated with two or more GCC countries) and international (defined as the presence of one or more author(s) affil- iated with a non-GCC country) collaboration was determined. As a measure of research quality, the imp- act factor of the publishing journal was obtained using the Journal Citation Reports tool (Clarivate Analytics, Phil- adelphia, Pennsylvania, USA).18 The number of citations per article was determined using the Scopus® database (Elsevier). The number of DFD-related articles from each GCC country per year was normalised according to the population size of the respective country for an estimation of the number of publications per million population (PPMP) per year.19,20 Collected data were entered into a pre-designed Excel spreadsheet, Version 2016 (Microsoft Corp., Red- mond, Washington, USA). Descriptive statistics were used to analyse the data. Comparisons were conducted using an independent samples Student’s t-test. The Cox- Stuart test was performed to identify significant trends over the investigated publication period. Statistical significance was based on a type I error rate of <5% (P <0.05). All analyses were performed using R Statist- ical Software (R Foundation for Statistical Computing, Vienna, Austria). Results A total of 105 publications from the GCC region were initially identified, of which six (5.7%) were excluded due to unrelated content (non-DFD-related research) and three (2.9%) due to article type (two letters and one case series). Of the remaining 96 articles, the vast majority (96.9%) focused on basic/clinical research. Only three (3.1%) RCTs were published, examining the effect of different treatments for chronic diabetic foot ulcers, peripheral neuropathy and wet gangrene prevention. These were published between 2013–2015 and had small sample sizes (23–112 patients). No systematic reviews/ meta-analyses were identified. Collaborative research was reported in 19 publications (19.8%), with one instance (5.3%) of local collaboration between Kuwait and the UAE, 16 cases (84.2%) of international collaboration and two (10.5%) involving both local and international collaboration. There were three (3.1%) international multicentre studies. None of the collaborative studies were RCTs. Overall, the number of publications per year showed a gradual yet significant upward trend, increasing from zero publications prior to 1991 to 15 in 2015 (P <0.01) [Figure 1]. The number of authors per publication also significantly increased during the study period (P = 0.02), with a median of three authors per publication. The country with the highest absolute number of publ- ications was Saudi Arabia (62.5%), followed by Kuwait (19.8%) and the UAE (7.3%). However, after adjusting for population, Kuwait had the highest PPMP per year (7.66), followed by Bahrain (4.55) and Qatar (3.85). There were no publications identified from Oman [Table 1]. Figure 1: Chart showing the number of diabetic foot disease-related publications per year originating from Gulf Cooperation Council countries between 1990–2015 (N = 96). There was a significant increase in publications per year during the study period (P <0.01). Ibrahim S. Al-Busaidi, Nadia N. Abdulhadi and Kirsten J. Coppell Clinical and Basic Research | e341 The articles were published in 65 different journals, of which the Saudi Medical Journal (9.4%) and Diabetes Research and Clinical Practice (4.2%) were most common. The majority of journals (72.3%) had only one published article. In total, 20 articles (20.8%) were published in GCC- based journals, including the Saudi Medical Journal, Bahrain Medical Bulletin, Journal of King Abdulaziz University - Medical Sciences, Annals of Saudi Medicine, Saudi Journal of Kidney Diseases & Transplantation and the Journal of Family & Community Medicine. Data regarding the impact factor of the publishing journal was only available for 52 articles (54.2%). The median impact factor was 0.15 ± 1.19 (range: 0–6.04). As of December 2015, the articles had a total of 1,097 citations, with an average of 11.43 citations per article (range: 0–98 citations). In total, 80 papers (83.3%) were cited at least once; however, 16 articles (16.7%) were uncited. Moreover, the five most cited articles represented 32.8% of all citations. The most frequently cited paper was a cross-sectional population-based study examining the prevalence of DM and its compl- ications in the UAE. The other four most cited articles were laboratory-based studies from Kuwait and Saudi Arabia related to the pathogenesis of diabetic wound healing and the bacteriology of diabetic foot infections [Table 2].21–25 Discussion Bibliometric analyses can help to identify trends in the quantity (i.e. publication output, areas of research focus and trends over time) and quality (i.e. the level of evidence, degree of collaboration, impact factor and citation rates) of published research.14,16 Such analyses are crucial when identifying gaps in knowledge and directing research efforts to answer pertinent unaddressed issues, whether on an international or local scale. In the present study, Kuwait was the most productive GCC country after adjusting for population size, while Oman had no publications during the study period. These findings are consistent with those of two other recent bibliometric analyses of biomedical and DFD- related publications from GCC countries.15,26 In the GCC region, DFD-related research has become a growing topic of interest among researchers. The current study observed a gradual but significant increase in the annual number of DFD-related publi- cations originating from GCC countries between 1990–2015, most noticeably from 2007 onwards. A Table 1: Country-specific rate of diabetic foot disease- related publications originating from Gulf Cooperation Council countries between 1990–2015 (N = 96) Country n (%) Population per year in millions* Estimated PPMP per year Bahrain 4 (4.2) 0.88 4.55 Kuwait 19 (19.8) 2.48 7.66 Oman 0 (0) 2.65 0.00 Qatar 4 (4.2) 1.04 3.85 Saudi Arabia 60 (62.5) 23.70 2.53 UAE 7 (7.3) 4.89 1.43 Total 94 (97.9)† 35.64 2.64 PPMP = publications per million population; UAE = United Arab Emirates. *Population data sourced from the World Bank.20 †Two publications were not included as they involved both local and international collaboration. Table 2: Most cited diabetic foot disease-related publications originating from Gulf Cooperation Council countries between 1990–2015 (N = 96)21–25 Author and year of publication Publication title Country Journal Number of citations* Saadi et al.21 (2007) Prevalence of diabetes mellitus and its complications in a population-based sample in Al Ain, United Arab Emirates UAE Diabetes Research and Clinical Practice 98 Bitar et al.22 (1996) Transforming growth factor-beta and insulin-like growth factor-I in relation to diabetes-induced impairment of wound healing Kuwait Journal of Surgical Research 86 Abdulrazak et al.23 (2005) Bacteriological study of diabetic foot infections Kuwait Journal of Diabetes and its Complications 74 El-Tahawy24 (2000) Bacteriology of diabetic foot Saudi Arabia Saudi Medical Journal 56 Bitar25 (1997) Insulin-like growth factor-1 reverses diabetes-induced wound healing impairment in rats Kuwait Hormone & Metabolic Research 46 UAE = United Arab Emirates. *Citation data sourced from the Scopus® database (Elsevier, Amsterdam, the Netherlands). Diabetic Foot Disease Research in Gulf Cooperation Council Countries A bibliometric analysis e342 | SQU Medical Journal, August 2018, Volume 18, Issue 3 number of factors could explain this observation. Before the 1990s, healthcare systems in the region were under- developed, with limited opportunities for medical education and minimal institutional support and investment in biomedical research.27 In addition, the health burden in GCC countries prior to 1990 was still dominated by infectious diseases.27,28 More recently, the burden of noncommunicable diseases has increased substantially in this region, thus prioritising DM research.9–12 Furthermore, politically-stable GCC counties have recently increased spending on research and development, along with the establishment of indep- endent organisations to fund biomedical research.26 In the current study, there was evidence of a growing body of basic/clinical research articles, incl- uding three RCTs published between 2013–2015. In addition, a considerable proportion of the published articles represented local or international collaboration and the number of authors per publication significantly increased over the study period. Both of these factors are indicators of the exchange of knowledge and research skills among researchers, reflecting a trend towards increasingly collaborative research. However, according to the Oxford Centre for Evidence-based Medicine, the three RCTs were classified as level 2 evidence, which is insufficient to change clinical practice.17 The findings of the present study indicated that the majority of the DFD-related publications originating from the GCC region were of poor quality, particularly in light of the low citation rate. The five most cited articles represented a relatively large proportion of all citations and were classified as level 3 or 4 evidence.17 Moreover, 20.8% of the articles were published in GCC- based journals, the majority of which are not MEDLINE®- indexed.29 Improving the quality of DFD-related research will require the provision of further training opportun- ities so that researchers in the GCC region can conduct impactful high-quality research.5 To this end, the alloc- ation of additional funding to support strategic research projects examining noncommunicable diseases in general, and DM specifically, is crucial. In the current study, the median journal impact factor of the publications was fairly low. However, the validity and utility of the impact factor as a measure of research quality has been vigorously debated.18,30,31 The value of published research to a specific population or in a certain context is not necessarily reflected by its publication in high-impact factor journals.32 It is possible that the authors may have deemed publication in a local journal more appropriate than in a higher-ranked international journal in light of the intended audience. Therefore, while the impact factor remains the most common and, arguably, the best existing metric for evaluating the bibliometric impact of published research to date, caution must be exercised when using it as the sole indicator of research quality and impact, especially for research originating from low-income countries and those with emerging economies.33 The current study was subject to several limitations. First, the methods used in the analysis may have under- estimated the publication rate of DFD-related research originating from GCC countries. As the search strategy was restricted to the MEDLINE® database (National Library of Medicine), articles published in journals not included in this database would have been omitted. Additionally, while publication in peer-reviewed journals is usually the preferred vehicle for the dissemination of medical research, it is possible that certain DFD-related studies, such as those conducted by governmental entities, may have been disseminated by other means (i.e. internal reports).13 Second, some article types not incl- uded in the analysis, such as reviews and case reports, may nevertheless represent valuable contributions to the literature. However, it is widely acknowledged that original research articles are an accurate reflection of research activity in a particular field and represent higher-quality evidence when compared to other types of publications.17 Finally, it was outside the scope of this study to estimate the contribution of GCC-researchers to international literature. Despite these limitations, the findings from this study are a reliable representation of GCC-based DFD-related research activity and may help to inform future efforts in this region. Conclusion The current study found that the number of DFD-related publications authored by GCC researchers increased significantly during the study period. Nevertheless, GCC countries lag behind other countries in terms of output and quality of DFD-related research, despite having some of the highest DM prevalence rates worldwide. This undoubtedly leaves gaps in knowledge related to the burden and management of DFD. Improving research funding and infrastructure and promoting local and international collaboration is crucial to enhancing DFD- related research in this region. c o n f l i c t o f i n t e r e s t The authors declare no conflicts of interest. f u n d i n g No funding was received for this study. Ibrahim S. Al-Busaidi, Nadia N. Abdulhadi and Kirsten J. Coppell Clinical and Basic Research | e343 References 1. International Diabetes Federation. IDF diabetes atlas: Seventh edition, 2015. From: http://diabetesatlas.org/resources/previous- editions.html Accessed: Mar 2018. 2. World Health Organization. Global Health Observatory (GHO) data: Country statistics. From: www.who.int/gho/countries/en/ Accessed: Mar 2018. 3. Ng SW, Zaghloul S, Ali HI, Harrison G, Popkin BM. The prev- alence and trends of overweight, obesity and nutrition-related non-communicable diseases in the Arabian Gulf States. Obes Rev 2011; 12:1–13. doi: 10.1111/j.1467-789X.2010.00750.x. 4. Klautzer L, Becker J, Mattke S. 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