==== Front BJR Open BJR Open bjro BJR Open 2513-9878 The British Institute of Radiology. BJRO-D-23-00027 10.1259/bjro.20230027 Review Article bjroBJRObrstBreastRadiographymriMRIpetPETultUltrasoundBibliometric analysis of the top 100 cited articles in breast radiology Top 100 most cited articles in breast radiology Ko and Tan Ko Tsz Ki BSc MBChB 1tszkiko95@gmail.com Tan Denise Jia Yun BSc (Hons) MBChB PgCert 2dtjy27@doctors.org.uk 1 College of Life Sciences, Leicester Medical School, George Davies Centre, Leicester, UK 2 Royal Wolverhampton Hospital Trust, Wolverhampton, UK Address correspondence to: Dr Tsz Ki Ko. E-mail: tszkiko95@gmail.com 2023 23 5 2023 5 1 2023002716 3 2023 17 4 2023 18 4 2023 © 2023 The Authors. Published by the British Institute of Radiology 2023 The Authors https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited. Objective: Bibliometrics analysis is a widely used approach that enables influential research within specific fields to be identified To identify the 100 most-cited articles in breast radiology and analyse the trend in breast imaging research. Methods and materials: A systematic search was conducted using the Thomson Rheuters Web of Science database. The results were ranked according to citation count and screened to create a single database. Data including first author, year of publication, journal, country of origin, primary institution, number of citations and average number of citations per year were extracted, as well as the impact factor and the 5-year impact factor of journals publishing the articles. Results: The systematic search yielded a total of 114,426 articles, after filters were applied to include papers that were available in English only. Citations for the 100 most-cited articles ranged from 515 to 3660. Half of the articles on the list were published between 2001 and 2010. Radiology has the most number of publications (n = 17), followed by JAMA-Journal of The American Medical Association (n = 9). CA-A Cancer Journal For Clinicians had the highest impact factor of 286.13. Mammogram (n = 49) was the most commonly studied modality, followed by Magnetic Resonance (n = 26). The most common topic of publication was diagnosis (n = 83). Conclusion: This research serves as a guide to the most influential articles on the topic of breast radiology. ==== Body pmcIntroduction Bibliometrics is a widely used approach that enables influential research within specific fields to be identified. 1 It is based upon statistical methods, which allows the reviewer to evaluate published papers and assess core parameters such as research performance, impact, and the productivity of key authors in the field. 2 In so doing, this style of research can be effective in identifying past trends within an area, and in enabling potential future directions to be identified in the process. 3 Because evidence-based practice is such an underpinning force within the field of healthcare provision, 4 the use of bibliometrics can therefore be both influential and impactful within the delivery of care to patients that is both safe and effective. 5 The use of bibliometrics has a strong precedence in the field of radiology, with bibliometric analysis having been applied both in the field of radiology as a whole 6 and within more specific subfields of the profession. 7 The recent bibliometric analysis conducted by Oo and Chu, 8 which focused on radiology of the head and neck was effective at producing a novel set of results that could have both clinical and research-related impact, and this work shall provide the framework for how this current study is conducted and reported. There is, to the best of this author’s knowledge, no bibliometric analysis that has been conducted on the issue of breast radiology, and so by providing a comprehensive assessment of this field, this current study shall seek to provide novel insights into this important area. Methods and materials A bibliometric analysis of the most highly cited articles in breast radiology was carried out in September 2022. A search was conducted within Thomson Reuters Web of Science (WOS) using the following key terms: Breast AND radiology OR Breast AND imaging OR Breast AND (X-ray OR radiograph) OR Breast AND mammogram OR Breast AND computed tomography OR Breast AND magnetic resonance OR Breast AND (ultrasound OR sonography) OR Breast AND interventional radiology OR Breast AND nuclear imaging OR Breast AND nuclear medicine This process returned a total of 145,396 articles. Filters were then applied to include full manuscripts that were available in English only (n = 114,426). The results were then sorted by the number of citations from the most-cited to the least-cited. This method was developed by Paladugu et.al 9 and was used in several other studies. Each article was manually screened for inclusion. Articles were included if they focused on diagnostic imaging, interpretation, imaging technique, utility and role of different imaging modalities or trends in breast radiology. Articles that focused on benign breast pathologies other than breast cancer were also included. Articles are excluded if they are not related to breast radiology, or if the primary focus was not on the breast. Articles that focus primarily on therapeutic radiology were excluded. Data such as WOS citations, year published, first author, last author, primary institution, country of origin, journal, journal impact factor, title, study design, study focus and modality were collected for each article and assembled into a single database (As shown in Figure 1). Figure 1. Flowchart depicting the selection of the top 100 most-cited articles on breast radiology Results The top 100 most-cited articles has a mean citation number of 899.41 and a median of 772, as shown in Table 1. The number of citations ranged from 515 to 3660. Table 1. The top 100 most-cited articles in breast radiology ranked in descending number of citations Rank Citations Average citations per year First author Publication year 1 3660 159.13 Rueckert, D 1999 2 2783 89.77 OPHIR, J 1991 3 1796 112.25 Xu, MH 2006 4 1740 102.35 Berry, DA 2005 5 1719 114.6 Saslow, D 2007 6 1701 94.5 Bercoff, J 2004 7 1551 41.92 TABAR, L 1985 8 1516 101.07 Boyd, NF 2007 9 1417 109 Anwar R. Padhani* 2009 10 1373 91.53 Koh, DM 2007 11 1368 72 Chlebowski, RT 2003 12 1334 121.27 Beard, P 2011 13 1325 57.61 Young, H 1999 14 1295 53.96 Krouskop, TA 1998 15 1288 92 Mettler, FA 2008 16 1238 45.85 STAVROS, AT 1995 17 1210 71.18 Pisano, ED 2005 18 1175 65.28 Kriege, M 2004 19 1171 73.19 Itoh, A 2006 20 1122 56.1 Kolb, TM 2002 21 1098 84.46 Calonge, N 2009 22 1070 89.17 Welch, HG 2010 23 1068 71.2 Soret, M 2007 24 1043 69.53 Einstein, AJ 2007 25 1040 80 Montaldo, G 2009 26 988 164.67 Siu, AL 2016 27 959 41.7 Kuhl, CK 1999 28 958 53.22 Berg, WA 2004 29 956 68.29 Berg, WA 2008 30 917 131 Oeffinger, KC 2015 31 917 61.13 Doi, K 2007 32 916 114.5 Plana, JC 2014 33 898 52.82 Kennedy, JE 2005 34 890 89 Marmot, MG 2012 35 886 88.6 Bleyer, A 2012 36 877 32.48 BOYD, NF 1995 37 864 43.2 Nightingale, K 2002 38 853 60.93 Willmann, JK 2008 39 843 49.59 Chen, J 2005 40 840 38.18 Phelps, ME 2000 41 835 75.91 DeSantis, C 2011 42 835 64.23 Nelson, HD 2009 43 834 41.7 Humphrey, LL 2002 44 834 30.89 KERLIKOWSKE, K 1995 45 821 45.61 Warner, E 2004 46 815 26.29 STRAUSS, LG 1991 47 795 37.86 Manduca, A 2001 48 790 39.5 Nystrom, L 2002 49 787 87.44 Bamber, J 2013 50 772 45.41 Leach, MO 2005 51 772 40.63 Carney, PA 2003 52 766 30.64 Garra, BS 1997 53 758 30.32 Schwartz, LM 1997 54 757 44.53 Kuhl, CK 2005 55 757 31.54 Elmore, G 1998 56 755 26.03 NYSTROM, L 1993 57 752 53.71 Fletcher, JW 2008 58 740 30.83 Sipkins, DA 1998 59 711 64.64 Bardhan, R 2011 60 710 29.58 Powles, T 1998 61 693 31.5 Mandelson, MT 2000 62 689 76.56 Cosgrove, D 2013 63 687 76.33 Skaane, P 2013 64 684 25.33 BYRNE, C 1995 65 681 68.1 Berg, WA 2012 66 670 134 Sigrist, RMS 2017 67 667 30.32 Ntziachristos, V 2000 68 667 22.23 BIRD, RE 1992 69 649 324.5 McKinney, SM 2020 70 631 21.76 FLETCHER, SW 1993 71 629 41.93 Lehman, CD 2007 72 623 24.92 Niklason, LT 1997 73 622 32.74 Swan, J 2003 74 620 18.79 KAISER, WA 1989 75 596 25.91 Ophir, J 1999 76 590 49.17 Sardanelli, F 2010 77 588 24.5 Boyd, NF 1998 78 586 27.9 Freer, TW 2001 79 581 20.75 PARKER, SH 1994 80 578 28.9 Fear, EC 2002 81 576 64 Ciatto, S 2013 82 575 19.17 Miller, AB 1992 83 571 31.72 Rohren, EM 2004 84 568 56.8 Berg, WA 2012 85 567 40.5 Houssami, N 2008 86 563 35.19 Shankar, LK 2006 87 556 25.27 Gotzsche, PC 2000 88 553 23.04 Borgstein, P 1998 89 550 27.5 Guo, Y 2002 90 549 68.63 Friedewald, SM 2014 91 549 24.95 Tromberg, BJ 2000 92 543 38.79 Tanter, M 2008 93 542 45.17 Dijkers, EC 2010 94 538 25.62 Orel, SG 2001 95 536 28.21 Smith, RA 2003 96 533 66.63 Angelo, M 2014 97 528 24 Meaney, PM 2000 98 522 34.8 Kuhl, C 2007 99 517 30.41 Elmore, JG 2005 100 515 42.92 Lee, CH 2010 Citations per year Citations per year ranged from 13.92 to 1830 with a mean of 84.74 and a median of 45.40 per year. The article by Rueckert et al 10 , titled ‘Nonrigid registration using free-form deformations: Application to breast MR images, is the most-cited article in the list and has the highest number of citations per year Year of publication The articles were published between 1985 and 2020. 2007 had the greatest number of publications, with eight articles, followed by the year 2005 with seven articles. Half of the articles on the list were published between 2001 and 2010 (Figure 2). Figure 2. Number of articles across time Most common first author There was a total of 92 first authors on the top 100 list. Amongst them, Berg has the highest number of articles, with four articles. There were five authors who were first authors of more than one article to the top 100 list. Journals The top 100 articles were published across 41 journals (Table 2). Radiology has the greatest number of publications (n = 17), followed by JAMA-Journal of The American Medical Association (n = 9). CA-A Cancer Journal For Clinicians had the highest impact factor of 286.13, the highest 5 year impact factor of 334.26 and the highest journal citation factor of 76.09, and it contributed to three articles on the list. Table 2. Journals in which the 100 top-cited articles in breast radiology were published Journal Number of articles Impact Factor (2021) 5 year impact factor Journal citation factor (2021) Total number of citations RADIOLOGY 17 29.146 17.483 5.52 1,3465 JAMA-JOURNAL OF THE AMERICAN MEDICAL ASSOCIATION 9 157.335 101.13 10.32 7686 NEW ENGLAND JOURNAL OF MEDICINE 7 176.079 125.115 22.26 7913 LANCET 7 202.731 130.838 21.81 6024 ANNALS OF INTERNAL MEDICINE 6 51.598 38.361 6.01 5285 JOURNAL OF THE NATIONAL CANCER INSTITUTE 5 11.816 13.993 2.28 3955 JOURNAL OF NUCLEAR MEDICINE 4 11.082 9.837 2.59 3198 CA-A CANCER JOURNAL FOR CLINICIANS 3 286.13 334.259 76.09 3090 PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2 12.779 13.45 2.61 1507 ULTRASONIC IMAGING 2 2 1.93 0.5 4078 IEEE TRANSACTIONS ON ULTRASONICS FERROELECTRICS AND FREQUENCY CONTROL 2 3.267 3.287 1.01 2731 NEOPLASIA 2 6.218 8.247 1.09 1966 EUROPEAN JOURNAL OF CANCER 2 10.002 9.433 1.72 1915 ULTRASOUND IN MEDICINE AND BIOLOGY 2 3.694 3.36 0.92 1407 ULTRASCHALL IN DER MEDIZIN 2 5.445 5.853 1.58 1476 JOURNAL OF CLINICAL ONCOLOGY 2 50.717 38.801 5.62 1324 NATURE MEDICINE 2 87.241 68.31 12.6 1273 IEEE TRANSACTIONS ON MEDICAL IMAGING 1 11.037 12.369 2.54 3660 REVIEW OF SCIENTIFIC INSTRUMENTS 1 1.843 1.751 0.4 1796 AMERICAN JOURNAL OF ROENTGENOLOGY 1 6.582 5.201 1.52 1373 INTERFACE FOCUS 1 4.661 5.338 1.09 1334 COMPUTERIZED MEDICAL IMAGING AND GRAPHICS 1 7.422 6.141 1.4 917 JOURNAL OF THE AMERICAN SOCIETY OF ECHOCARDIOGRAPHY 1 7.722 8.357 1.28 916 NATURE REVIEWS CANCER 1 69.8 78.98 7.95 898 NATURE REVIEWS DRUG DISCOVERY 1 112.288 98.74 9.68 853 NANO LETTERS 1 12.262 12.709 1.95 843 MEDICAL IMAGE ANALYSIS 1 13.828 14.934 2.48 795 ACCOUNTS OF CHEMICAL RESEARCH 1 24.466 24.462 1.38 711 THERANOSTICS 1 11.6 12.201 2.52 670 NATURE 1 69.504 63.58 10.88 649 CANCER 1 6.921 7.802 1.22 622 CANCER EPIDEMIOLOGY BIOMARKERS & PREVENTION 1 4.09 5.594 0.98 588 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING 1 4.756 5.674 1.16 578 LANCET ONCOLOGY 1 54.433 49.204 8.48 576 CANADIAN MEDICAL ASSOCIATION JOURNAL 1 16.859 14.14 2.04 575 JOURNAL OF THE AMERICAN COLLEGE OF SURGEONS 1 6.532 6.163 2.51 553 JOURNAL OF MAGNETIC RESONANCE IMAGING 1 5.119 4.801 1.21 550 CLINICAL PHARMACOLOGY & THERAPEUTICS 1 6.903 7.038 1.65 542 IEEE TRANSACTIONS ON MICROWAVE THEORY AND TECHNIQUES 1 4.381 4.348 1.12 528 JOURNAL OF THE AMERICAN COLLEGE OF RADIOLOGY 1 6.24 5.947 1.29 515 PROCEEDINGS OF THE INSTITUTION OF MECHANICAL ENGINEERS PART H-JOURNAL OF ENGINEERING IN MEDICINE 1 1.763 1.871 0.33 596 Country and institution of origin The United States (USA) has the greatest number of publications on the list (n = 61), followed by the United Kingdom (UK) (n = 12). The results are displayed in Figure 3. In terms of the affiliated academic institutions of the first authors on the list, Stanford University and the University of Washington both have the highest number of articles, with four each. Figure 3. Country of the first author for 100 top-cited articles in breast radiology Study design The majority of the study designs was prospective (n = 60), followed by reviews (n = 28), retrospective (n = 10) and a mix of prospective and retrospective (n = 2) (Table 3) Table 3. Study designs of included papers Descriptor Frequency (n) Study design Prospective 60 Review 28 Retrospective 10 Mixed 2 Modality (15 articles focused on more than one modality) Mammogram 49 MR 26 Ultrasound 26 PET 10 CT 5 Others 5 Primary topic/ focus Diagnosis 83 Prognosis 1 Treatment response 3 Management 2 Others 11 Related to breast cancer Yes 90 No 10 Topic Imaging modality, primary topic of the article and if the article was breast cancer-related were also evaluated for all of the articles on the list—83 of them focused on the diagnosis of breast pathology and 90 papers are related to breast cancer (Table 3) Discussion This bibliometric analysis offers a range of interesting insights into the field of breast radiology. These findings include, as presented above, insights into how this field has developed over the years, and what the core focuses have been over time. From the analysis conducted as part of this current study, the most-cited article in this field was the work of Rueckert and colleagues, which was published in the journal IEEE Transactionson Medical Imaging in 1999. This article has, at the time of conducting this analysis, received n = 3660 total citations. This, averaged across the 23 years since publication equates to approximately n = 159 citations being made of this paper every year; clearly indicating therefore that Rueckert and colleagues’ work continues to have a lasting and influential impact on the field of breast radiology. It should be noted that this paper, as with the second most-cited article in this field—that of Ophir et al 11 —was published before the turn of the century. Because of the way that bibliometric analysis works, this can tend to bias earlier published work towards appearing more influential. 12 However, whilst this caveat should be borne in mind, the scale of influence that these papers had is incontrovertible. The top three journals within this current analysis—Radiology; JAMA-Journal of the American Medical Association; and the New England Journal of Medicine—are not all journals which focus specifically on the field of radiology; indeed, only Radiology, with a total of n = 17 articles within this bibliometric analysis is focussed on this topic. This is a finding of interest because this does not support the findings of Oo and Chu, 8 who noted that in their analysis of head and neck radiology, the top three journals were all radiology-centric in nature. The reasons for the disparity between the findings of Oo and Chu 8 and those of this current bibliometric analysis may be the subject matter, with the issue of breast cancer, in particular, being considered more feasible or of interest to a wider, more general audience. Next to be discussed is the journal impact factor of the journals within the top 100 list presented above. The impact factor of a journal is a blunt, yet influential approximation of the esteem and influence of that journal, 13 which is calculated by dividing the citations of papers in that journal across the period of a year by the number of articles published in the previous 2 years. 13 The higher the impact factor is, the more influential that journal is considered to be, 14 and it is notable that the impact factor of the above, top three journals ranges considerably. For example, the impact factor for the journal Radiology is 29.1, whilst the second-ranked journal of JAMA-Journal of the American Medical Association (impact factor = 157.3) and third-ranked journal of New England Journal of Medicine (impact factor = 176.1) are far more influential. This again may indicate why breast radiology researchers targeted these journals for publishing their studies, due to the greater reach and impact of such journals. It is also notable that, regarding the location of study, the 83% of the included papers were published by American or British research teams, with the vast majority of these—n = 61—being based in America. This is indicative of the research culture across clinical teams in these countries, and the resources available to clinical and research teams to develop the evidence base. This finding is highly conducive with those of other bibliometric analyses published in the field of radiology. 15 From the analysis conducted as part of this current study, it is clear that the core focus in the field of breast radiology is breast cancer, with 90 papers within the selected 100 addressing this issue. This can potentially be related to the emotive nature of breast cancer 16 and the impact that this awareness has on research funding decisions and opportunities. 17 Whilst this is important in one sense—clearly it can be argued that the advances made in understanding breast cancer screening, identification and treatment can be attributed to the huge research resources provided to this area 18 —it is possible that this focus has limited advances in other areas of breast radiology. It is however notable that the volume of studies included in this bibliometric analysis peaked between 2001 and 2015, which may either indicate a shift in focus of research teams in recent years, or alternatively may be indicative of the primacy biases that are inherent within bibliometric analysis studies. 12 Whilst nearly half of studies focussed on a primary modality of mammograms, this is indicative of practice in this field, although it should be noted that other core approaches such as PET or CT scans tend to be underrepresented within the top 100-cited articles in this area, and more perhaps needs to be done to address this imbalance. It is also notable that n = 60 of these studies were prospectively designed; this is important to address because unlike in retrospectively designed work, such studies are able to limit the potential of biases and confounding variables to influence findings. 19 The rigour of these selected works is further underlined by the relatively high volume of review studies (n = 28). Well-conducted reviews can take into account important issues such as risk of bias within primary studies, 20 and as such are considered to be near the apex of the evidence-based pyramid within healthcare research. 21 As far as this author is aware, this is the first bibliometric analysis to have focused on the issue of breast radiology. This study has therefore produced a set of novel results that can provide researchers, radiologists, and other allied health professionals with information about the most impactful. Influential papers within this field, which in turn may inform both their approach to practice, and potential directions for future research projects. However, whilst this work is therefore likely to be influential in the above ways, it should be noted that there are a number of limitations associated with this study. It is important that these limitations are discussed in order for there to be a transparent discussion of the implications from this work. For example, it is possible that the search terms used incorporated some form of researcher bias into the search process. 8 It is also of note that articles which focussed on therapeutic radiology were excluded from consideration for this analysis, which may have biased the inclusion of papers within this work; a future bibliometric analysis into therapeutic radiology may help redress this imbalance. Finally, this bibliometric analysis utilised output from WOS, but as noted in the past bibliometric analysis, 8 citation data can differ considerably across core databases such as WOS, Google Scholar, PubMed or Scopus. However, whilst these limitations should be held in mind, it should also be noted that a central bias of this methodology—that towards earlier published papers—was addressed via the use of a citations per year metric, which is indicative of this work being rigorously conducted and transparent in nature. In conclusion, this study has provided a detailed and comprehensive overview of the top 100 most-cited papers in the field of breast radiology. In so doing, this study can provide core insights for both clinicians and researchers alike, and lead them to understand the most influential papers within this important field. It is anticipated that this may positively impact on the way that this area is addressed in the future, and that the evidence base in this field can be further advanced as a result. Competing interests: The authors declare that they have no competing interests Ethics approval: Not applicable Contributors: Both DJYT and TKK contributed equally in conceptualisation, data curation, formal analysis, investigation and methodology section of the manuscript. Both authors have equal parts in project administration, writing draft, reviewing, and editing the manuscript. ==== Refs REFERENCES 1. Godin B . On the origins of bibliometrics. Scientometrics 2006; 68 : 109–33. doi: 10.1007/s11192-006-0086-0 2. Cooper ID . Bibliometrics basics. J Med Libr Assoc 2015; 103 : 217–18. doi: 10.3163/1536-5050.103.4.013 26512226 3. McBurney MK , Novak PL. What is bibliometrics and why should you care?. 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