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. 2017 Nov 3;90(1080):20160755. doi: 10.1259/bjr.20160755

Trends in CT colonography: bibliometric analysis of the 100 most-cited articles

Mohammed Fahim Mohammed 1,2,1,2, Tejbir Chahal 3, Bo Gong 3, Nizar Bhulani 4, Michael O’Keefe 1,5,1,5, Timothy O’Connell 1, Savvas Nicolaou 1, Faisal Khosa 1
PMCID: PMC6047654  PMID: 28972802

Abstract

Our purpose was to identify the top 100 cited articles, which focused on CT colonography (CTC). This list could then be analysed to establish trends in CTC research while also identifying common characteristics of highly cited works. Web of Science search was used to create a database of scientific journals using our search terms. A total of 10,597 articles were returned from this search. Articles were included if they focused on diagnostic imaging, imaging technique, cost-effectiveness analysis, clinical use, patient preference or trends in CTC. Articles were ranked by citation count and screened by two attending radiologists. The following information was collected from each article: database citations, citations per year, year published, journal, authors, department affiliation, study type and design, statistical analysis, sample size, modality and topic. Citations for the top 100 articles ranged from 73 to 1179, and citations per year ranged from 4.5 to 84.21. Articles were published across 22 journals, most commonly Radiology (n = 37) and American Journal of Roentgenology (n = 19). Authors contributed from 1 to 20 articles. 19% of first authors were affiliated with a department other than radiology. Of the 100 articles, the most common topics were imaging technique (n = 40), diagnostic utility of imaging (n = 28) and clinical uses (n = 18). Our study provides intellectual milestones in CTC research, reflecting on the characteristics and quality of published literature. This work also provides the most influential references related to CTC and serves as a guide to the features of a citable paper in this field.

Introduction

Bibliometric is the statistical analysis of publications and medical literature. Methods of bibliometrics are used in academic fields to provide analysis of scientific literature. It is used by researchers to explore the impact of their field, of a set of researchers or of a certain publication.1,2 Bibliometrics has a range of applications and its impact continues to soar within the scientific community.

Bibliometrics analyses both qualitative and quantitative data within publications and a major strength is its ability to scrutinize citation analysis. Citation analysis examines publications to identify the amount of impact they have on their respective fields.1–4 Bibliometric analyses are very useful for identifying trends in literature and future research directions.1 The role of bibliometric analysis in academic medicine is expected to grow with time.4

The most-cited articles in radiology or radiology subspecialties have been collected many times for publication.5–18 Also, many of the 100 most-cited articles in radiology or radiology journals are found through a simple search.5,6,11,14–17 Some of these studies focused solely on the top 100 cited articles in radiology.5,11,14 These employed different methods to compile their citation list, yet there was a significant overlap in their final compilation.5,11,14 All three studies restricted their literature search to radiology-specific journals and cited it as a limitation.5,11,14

Our literature search did not reveal bibliometric analyses of the 100 most-cited articles in CT colonography (CTC). These focused bibliometric analyses have implications for clinical radiologists and researchers examining recent trends in publications on a specific entity.

The purpose of this study was to recognize and examine the top 100 cited articles in which CTC was used across all peer-reviewed scientific journals. We included CTC articles published in non-radiology journals including but not limited to the New England Journal of Medicine, Lancet and JAMA, creating a comprehensive database of the most influential articles that utilize this imaging technique. This paper identifies the most influential publications and authors to date in CTC, while also recognizing current and future research directions.

Methods and Materials

To conduct a bibliometric analysis of the most highly cited articles in CTC, we performed a search of Thomson Reuters' Web of Science (WOS) All Databases on 25 July 2016, which indexed over 12,000 of the most-cited journals in the world. All journals in the search engine were included regardless of country of origin or medical specialty. We used the following search phrase in a “topic” search, without restriction of language or publication year:

  • (Computed Colonography) OR (Computed Colonoscopy) OR (Computed Colography) OR (Computed Coloscopy).

  • OR (Virtual Colonography) OR (Virtual Colonoscopy) OR (Virtual Colography) OR (Virtual Coloscopy).

  • OR (Computed Tomographic Colonography) OR (Computed Tomographic Colonoscopy) OR (Computed Tomographic Colography) OR (Computed Tomographic Coloscopy).

  • OR (CT Colonography) OR (CT Colonoscopy) OR (CT Colography) OR (CT Coloscopy).

A total of 10,597 articles were returned from this search, and included all articles in our search, regardless of language. Once the results were compiled, a single list was created which ranked articles from most to least cited. Beginning with the most highly cited article, each publication was assessed for inclusion. Articles were included if they focused on diagnostic imaging outcome/interpretation (comparison with another modality, sensitivity/specificity/PPV/NPV), CTC imaging technique, cost effectiveness analysis, clinical use of CTC, patient preference or trends in CTC. Articles were excluded if they did not pertain to CTC, or explored laboratory or basic science research.

We then compiled the most-cited articles into a single database. Citation count was acquired from WOS, WOS core collection and Scopus. In case of occasional variability in the citation counts we used WOS, which has show most reliable for clinical medicine.2,19,20 The database included: WOS citations, citations per year, year published, journal, authors, department affiliation, study type and design, statistical analysis, sample size, modality and topic, with WOS providing the reference source for our chosen metrics in case of discrepancies with Scopus®. Impact factors for journals were determined from Thomson Reuters Journal Citation Reports issued in 2015.

Results

Citations for the top 100 articles ranged from 73 to 1179 with a median of 120.5. These results are displayed below in Table 1.

Table 1.

The 100 top-cited articles in CTC GI imaging ranked in descending order of number of citations

Rank Article Citations
1. Pickhardt PJ, Choi JR, Hwang I, Butler JA, Puckett ML, Hildebrandt HA, et al. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med 2003; 349(23): 2191–2200doi:10.1056/NEJMoa031618 1179
2. Fenlon HM, Nunes DP, Schroy PC, Barish MA, Clarke PD, Ferrucci JT. A comparison of virtual and conventional colonoscopy for the detection of colorectal polyps. N Engl J Med 1999; 341(20): 1496–1503. doi:10.1056/nejm199911113412003 515
3. Johnson CD, Chen MH, Toledano AY, Heiken JP, Dachman A, Kuo MD, et al. Accuracy of CT colonography for detection of large adenomas and cancers. N Engl J Med 2008; 359(12): 1207–1217doi:10.1056/NEJMoa0800996 498
4. Cotton PB, Durkalski VL, Benoit PC, Palesch YY, Mauldin PD, Hoffman B, et al. Computed tomographic colonography (virtual colonoscopy) - A multicenter comparison with standard colonoscopy for detection of colorectal neoplasia. J Am Med Assoc 2004; 291(14): 1713–1719. doi:10.1001/jama.291.14.1713 445
5. Rockey DC, Poulson E, Niedzwiecki D, Davis W, Bosworth HB, Sanders L, et al. Analysis of air contrast barium enema computed tomographic colonography, and colonoscopy: prospective comparison. Lancet 2005; 365(9456): 305–311. 372
6. Yee J, Akerkar GA, Hung RK, Steinauer-Gebauer AM, Wall SD, McQuaid KR. Colorectal neoplasia: performance characteristics of CT colonography for detection in 300 patients. Radiology 2001; 219(3): 685–692. 360
7. Kim DH, Pickhardt PJ, Taylor AJ, Leung WK, Winter TC, Hinshaw JL, et al. CT colonography versus colonoscopy for the detection of advanced neoplasia. N Engl J Med 2007 357(14): 1403–1412. doi:10.1056/NEJMoa070543 353
8. Zalis ME, Barish MA, Choi JR, Dachman AH, Fenlon HM, Ferrucci JT, et al. CT colonography reporting and data system: a consensus proposal. Radiology 2005; 236(1): 3–9. doi:10.1148/radiol.2361041926 321
9. Fletcher JG, Johnson CD, Welch TJ, MacCarty RL, Ahlquist DA, Reed JE, et al. Optimization of CT colonography technique: prospective trial in 180 patients. Radiology 2000; 216(3): 704–711. 243
10. Hara AK, Johnson CD, Reed JE, Ahlquist DA, Nelson H, MacCarty RL, et al. Detection of colorectal polyps with CT colography: initial assessment of sensitivity and specificity. Radiology 1997; 205(1): 59–65. 240
11. Johnson CD, Harmsen WS, Wilson LA, MacCarty RL, Welch TJ, Ilstrup DM, et al. Prospective blinded evaluation of computed tomographic colonography for screen detection of colorectal polyps. Gastroenterology 2003; 125(2): 311–319. doi:10.1016/s0016-5085 (03)00894–1 240
12. Yoshida H, Nappi J. Three-dimensional computer-aided diagnosis scheme for detection of colonic polyps. IEEE Trans Med Imag 2001; 20(12): 1261–1274. doi:10.1109/42.974921 225
13. Mulhall BP, Veerappan GR, Jackson JL. Meta-analysis: computed tomographic colonography. Ann Intern Med 2005; 142(8): 635–650. 218
14. Hara AK, Johnson CD, MacCarty RL, Welch TJ. Incidental extracolonic findings at CT colonography. Radiology 2000; 215(2): 353–357. 213
15. Halligan S, Altman DG, Taylor SA, Mallett S, Deeks JJ, Bartram CI, et al. CT colonography in the detection of colorectal polyps and cancer: systematic review meta-analysis and proposed minimum data set for study level reporting. Radiology 2005; 237(3): 893–904. doi:10.1148/radiol.2373050176 210
16. Dachman AH, Kuniyoshi JK, Boyle CM, Samara Y, Hoffmann KR, Rubin DT, et al. CT colonography with three-dimensional problem solving for detection of colonic polyps. Am J Roentgenol 1998; 171(4): 989–995. 208
17. Summers RM, Johnson CD, Pusanik LM, Malley JD, Youssef AM, Reed JE. Automated polyp detection at CT colonography: feasibility assessment in a human population. Radiology 2001; 219(1): 51–59. 196
18. Gluecker TM, Johnson CD, Harmsen WS, Offord KP, Harris AM, Wilson LA, et al. Colorectal cancer screening with CT colonography, colonoscopy, and double-contrast barium enema examination: prospective assessment of patient perceptions and preferences. Radiology 2003; 227(2): 378–384. doi:10.1148/radiol.2272020293 195
19. Lefere P, Gryspeerdt S, Marrannes J, Baekelandt M, Van Holsbeeck B. CT colonography after fecal tagging with a reduced cathartic cleansing and a reduced volume of barium. American Journal of Roentgenology 2005;184(6): 1836–1842. 191
20. Iannaccone R, Laghi A, Catalano C, Mangiapane F, Lamazza A, Schillaci A, et al. Computed tomographic colonography without cathartic preparation for the detection of colorectal polyps. Gastroenterology 2004; 127(5): 1300–1311doi:10.1053/j.gastro.2004.08.025 186
21. Callstrom MR, Johnson CD, Fletcher JG, Reed JE, Ahlquist DA, Harmsen WS, et al. CT colonography without cathartic preparation: feasibility study. Radiology 2001; 219(3): 693–698. 182
22. Fenlon HM, McAneny DB, Nunes DP, Clarke PD, Ferrucci JT. Occlusive colon carcinoma: Virtual colonoscopy in the preoperative evaluation of the proximal colon. Radiology 1999; 210(2): 423–428. 179
23. Graser A, Stieber P, Nagel D, Schafer C, Horst D, Becker CR, et al. Comparison of CT colonography colonoscopy, sigmoidoscopy and faecal occult blood tests for the detection of advanced adenoma in an average risk population. Gut 2009; 58(2): 241–248. doi:10.1136/gut.2008.156448 179
24. Hara AK, Johnson CD, Reed JE, Ahlquist DA, Nelson H, Ehman RL, et al. Detection of colorectal polyps by computed tomographic colography: feasibility of a novel technique. Gastroenterology 1996; 110(1): 284–290. doi:10.1053/gast.1996.v110.pm8536869 176
25. Summers RM, Beaulieu CF, Pusanik LM, Malley JD, Jeffrey RB, Glazer DI, et al. Automated polyp detector for CT colonography: feasibility study. Radiology 2000; 216(1): 284–290. 174
26. Summers RM, Yao JH, Pickhardt PJ, Franaszek M, Bitter I, Brickman D, et al. Computed tomographic virtual colonoscopy computer-aided polyp detection in a screening population. Gastroenterology 2005; 129(6): 1832–1844. doi:10.1053/j.gastro.2005.08.054 173
27. Johnson CD, Dachman AH. CT colonography: the next colon screening examination? Radiology 2000; 216(2): 331–341. 172
28. Hara AK, Johnson CD, Reed JE, Ehman RL, Ilstrup DM. Colorectal polyp detection with CT colography: two- versus three-dimensional techniques - Work in progress. Radiology 1996; 200(1): 49–54. 170
29. Yoshida H, Nappi J, MacEneaney P, Rubin DT, Dachman AH. Computer-aided diagnosis scheme for detection of polyps at CT colonography. Radiographics 2002; 22(4): 963–979. 160
30. Svensson MH, Svensson E, Lasson A, Hellstrom M. Patient acceptance of CT colonography and conventional colonoscopy: Prospective comparative study in patients with or suspected of having colorectal disease. Radiology 2002; 222(2): 337–345. doi:10.1148/radiol.2222010669 158
31. Chen SC, Lu DSK, Hecht JR, Kadell BM. CT colonography: value of scanning in both the supine and prone positions. Am J Roentgenol 1999; 172(3): 595–599. 152
32. Sonnenberg A, Delco F, Bauerfeind P. Ts virtual colonoscopy a cost-effective option to screen for colorectal cancer? Am J Gastroenterol 1999; 94(8): 2268–2274. 152
33. Macari M, Bini EJ, Xue XN, Milano A, Katz SS, Resnick D, et al. Colorectal neoplasms: prospective comparison of thin-section low-dose multi-detector row CT colonography and conventional colonoscopy for detection. Radiology 2002; 224(2): 383–392. doi:10.1148/radiol.2242011382 149
34. Gluecker TM, Johnson CD, Wilson LA, MacCarty RL, Welch TJ, Vanness DJ, Ahlquist DA. Extracolonic findings at CT colonography: Evaluation of prevalence and cost in a screening population. Gastroenterology 2003; 124(4): 911–916. doi:10.1053/gast.2003.50158 148
35. Paik DS, Beaulieu CF, Rubin GD, Acar B, Jeffrey RB, Yee J, et al. Surface normal overlap: A computer-aided detection algorithm with application to colonic polyps and lung nodules in helical CT. IEEE Trans Med Imag 2004; 23(6): 661–675. doi:10.1109/tmi.2004.826362 147
36. Lieberman D, Nadel M, Smith RA, Atkin W, Duggirala SB, Fletcher R, et al. Standardized colonoscopy reporting and data system: report of the Quality Assurance Task Group of the National Colorectal Cancer Roundtable. Gastrointest Endosc 2007; 65(6): 757–766. doi:10.1016/j.gie.2006.12.055 146
37. Royster AP, Fenlon HM, Clarke PD, Nunes DP, Ferrucci JT. CT colonoscopy of colorectal neoplasms: two-dimensional and three-dimensional virtual-reality techniques with colonoscopic correlation. Am J Roentgenol 1997; 169(5): 1237–1242. 146
38. Rex DK, Vining D, Kopecky KK. An initial experience with screening for colon polyps using spiral CT with and without CT colography (virtual colonoscopy). Gastrointest Endosc 1999; 50(3): 309–313. doi:10.1053/ge.1999.v50.97776 141
39. Morrin MM, Kruskal JB, Farrell RJ, Goldberg SN, McGee JB, Raptopoulos V. Endoluminal CT colonography after an incomplete endoscopic colonoscopy. Am J Roentgenol 1999; 172(4): 913–918. 136
40. Brenner DJ, Georgsson MA. Mass screening with CT colonography: Should the radiation exposure be of concern? Gastroenterology 2005; 129(1): 328–337. doi:10.1053/j.gastro.2005.05.021 135
41. Ristvedt SL, McFarland EG, Weinstock LB, Thyssen EP. Patient preferences for CT colonography conventional colonoscopy and bowel preparation. Am J Gastroenterol 2003; 98(3): 578–585. doi:10.1016/s0002-9270 (02)06024–0 133
42. Macari M, Milano A, Lavelle M, Berman P, Megibow AJ. Comparison of time-efficient CT colonography with two- and three-dimensional colonic evaluation for detecting colorectal polyps. Am J Roentgenol 2000;174(6): 1543–1549. 129
43. Morrin MM, Farrell RJ, Kruskal JB, Reynolds K, McGee JB, Raptopoulos V. Utility of intravenously administered contrast material at CT colonography. Radiology 2000; 217(3): 765–771. 129
44. Pineau BC, Paskett ED, Chen GJ, Espeland MA, Phillips K, Han JP, et al. Virtual colonoscopy using oral contrast compared with colonoscopy for the detection of patients with colorectal polyps. Gastroenterology 2003; 125(2): 304–310. doi:10.1016/s0016-5085 (03)00885–0 127
45. Hara AK, Johnson CD, MacCarty RL, Welch TJ, McCollough CH, Harmen WS. CT colonography: single-versus multi-detector row imaging. Radiology 2001;219(2): 461–465. 125
46. Van Gelder RE, Nio CY, Florie J, Bartelsman JF, Snel P, De Jager SW, et al. Computed tomographic colonography compared with colonoscopy in patients at increased risk for colorectal cancer. Gastroenterology 2004; 127(1): 41–48. doi:10.1053/j.gastro.2004.03.055 124
47. Flicek KT, Hara AK, Silva AC, Wu Q, Peter MB, Johnson CD. Reducing the radiation dose for CT colonography using adaptive statistical iterative reconstruction: A pilot study. Am J Roentgenol 2010; 195(1): 126–131. doi:10.2214/ajr.09.3855 122
48. Pickhardt PJ, Choi JHR. Electronic cleansing and stool tagging in CT colonography: Advantages and pitfalls with primary three-dimensional evaluation. Am J Roentgenol 2003; 181(3): 799–805. 122
49. Pickhardt PJ, Hassan C, Laghi A, Zullo A, Kim DH, Morini S. Cost-effectiveness of colorectal cancer screening with computed tomography colonography - The impact of not reporting diminutive lesions. Cancer 2007; 109(11): 2213–2221doi:10.1002/cncr.22668 121
50. van Gelder RE, Venema HW, Serlie IWO, Nio CY, Determann RM, Tipker CA, et al. CT colonography at different radiation dose levels: Feasibility of dose reduction. Radiology 2002; 224(1): 25–33. doi:10.1148/radiol.2241011126 121
51. Macari M, Berman P, Dicker M, Milano A, Megibow AJ. Usefulness of CT colonography in patients with incomplete colonoscopy. Am J Roentgenol 1999; 173(3): 561–564. 120
52. Hara AK, Johnson CD, Reed JE, Ahlquist DA, Nelson H, Ehman RL, Harmsen WS. Reducing data size and radiation dose for CT colonography. Am J Roentgenol 1997; 168(5): 1181–1184. 116
53. Regge D, Laudi C, Galatola G, Della Monica P, Bonelli L, Angelelli G, et al. Diagnostic accuracy of computed tomographic colonography for the detection of advanced neoplasia in individuals at increased risk of colorectal cancer. J Am Med Assoc 2009; 301(23): 2453–2461. 115
54. Pickhardt PJ, Hassan C, Halligan S, Marmo R. Colorectal Cancer: CT colonography and colonoscopy for detection-systematic review and meta-analysis. Radiology 2011; 259(2): 393–405. doi:10.1148/radiol.11101887 113
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56. Spinzi G, Belloni G, Martegani A, Sangiovanni A, Del Favero C, Minoli G. Computed tomographic colonography and conventional colonoscopy for colon diseases: a prospective blinded study. Am J Gastroenterol 2001; 96(2): 394–400. 111
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59. Sosna J, Morrin MM, Kruskal JB, Lavin PT, Rosen MP, Raptopoulos V. CT Colonography of colorectal polyps: a metaanalysisAm J Roentgenol 2003; 181(6): 1593–1598. 106
60. Macari M, Lavelle M, Pedrosa I, Milano A, Dicker M, Megibow AJ, Xue XN. Effect of different bowel preparations on residual fluid at CT colonography. Radiology 2001; 218(1): 274–277. 105
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63. Burling D, Halligan S, Slater A, Noakes MJ, Taylor SA. Potentially serious adverse events at CT colonography in symptomatic patients: National survey of the United Kingdom. Radiology 2006; 239(2): 464–471. doi:10.1148/radiol.2392051101 103
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65. Zalis ME, Hahn PF. Technical innovationDigital subtraction bower cleansing in CT colonographyAm J Roentgenol 2001; 176(3): 646–648. 101
66. Fidler JL, Johnson CD, MacCarty RL, Welch TJ, Hara AK, Harmsen WS. Detection of flat lesions in the colon with CT colonography. Abdom Imaging 2002; 27(3): 292–300. doi:10.1007/s00261-001-0171-z 100
67. Filippone A, Ambrosini R, Fuschi M, Marinelli T, Genovesi D, Bonomo L. Preoperative T and N staging of colorectal cancer: accuracy of contrast-enhanced multi-detector row CT colonography - Initial experience. Radiology 2004; 231(1): 83–90. doi:10.1148/radiol.2311021152 99
68. Pickhardt PJ, Hanson ME, Vanness DJ, Lo JY, Kim DH, Taylor AJ, et al. Unsuspected extracolonic findings at screening CT colonography: clinical and economic impact. Radiology 2008; 249(1): 151–159. doi:10.1148/radiol.2491072148 98
69. Pickhardt PJ. Incidence of colonic perforation at CT colonography: Review of existing data and implications for screening of asymptomatic adults. Radiology 2006; 239(2): 313–316. doi:10.1148/radiol.2392052002 97
70. van Gelder RE, Birnie E, Florie J, Schutter MP, Bartelsman JF, Snel P, et al. CT colonography and colonoscopy: assessment of patient preference in a 5 week follow-up study. Radiology 2004; 233(2): 328–337. doi:10.1148/radiol.2331031208 97
71. Pickhardt PJ, Nugent PA, Choi JR, Schindler WR. Flat colorectal lesions in asymptomatic adults: Implications for screening with CT virtual colonoscopy. Am J Roentgenol 2004; 183(5): 1343–1347. 96
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74. Yee J, Hung RK, Akerkar GA, Wall SD. The usefulness of glucagon hydrochloride for colonic distention in CT colonography. Am J Roentgenol 1999; 173(1): 169–172. 93
75. Iannaccone R, Laghi A, Catalano C, Brink JA, Mangiapane F, Trenna S, et al. Detection of colorectal lesions: lower-dose multi-detector row helical CT colonograph compared with conventional colonoscopy. Radiology 2003; 229(3): 775–781. doi:10.1148/radiol.2293021399 92
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78. Ferrucci JT. Colon cancer screening with virtual colonoscopy: Promise polyps politics. Am J Roentgenol 2001; 177(5): 975–988. 89
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88. Pickhardt PJ, Taylor AJ, Kim DH, Reichelderfer M, Gopal DV, Pfau PR. Screening for colorectal neoplasia with CT colonography: initial experience from the 1 st year of coverage by third-party payers. Radiology 2006; 241(2): 417–425. doi:10.1148/radiol.2412052007 86
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90. Johnson CD, Toledano AY, Herman BA, Dachman AH, McFarland EG, Barish MA, et al. Computerized tomographic colonography: performance evaluation in a retrospective multicenter setting. Gastroenterology 2003; 125(3): 688–695. doi:10.1016/s0016-5085 (03)01058–8 83
91. Zalis ME, Perumpillichira J, Del Frate C, Hahn PF. CT colonography: digital subtraction bowel cleansing with mucosal reconstruction - Initial observations. Radiology 2003; 226(3): 911–917. doi:10.1148/radiol.2263012059 83
92. Fletcher JG, Johnson CD, MacCarty RL, Welch TJ, Reed JE, Hara AK. CT colonography: potential pitfalls and problem-solving techniques. Am J Roentgenol 1999; 172(5): 1271–1278. 81
93. Taylor SA, Halligan S, Burling D, Morley S, Bassett P, Atkin W, Bartram CI. CT colonography: effect of experience and training on reader performance. Eur Radiol 2004; 14(6): 1025–1033. doi:10.1007/s00330-004-2262-z 79
94. Vijan S, Hwang I, Inadomi J, Wong RKH, Choi JR, Napierkowski J, et al. The cost-effectiveness of CT colonography in screening for colorectal neoplasiaAm J Gastroenterol 2007; 102(2): 380–390doi:10.1111/j.1572–0241.2006.00970.x 78
95. Ladabaum U, Song K, Fendrick AM. Colorectal Neoplasia Screening With Virtual Colonoscopy: When at What Cost and With What National Impact? Clin Gastroenterol Hepatol 2004; 2(7): 554–563. doi:10.1053/s1542-3565 (04)00247–2 77
96. Lefere PA, Gryspeerdt SS, Dewyspelaere J, Baekelandt M, Van Holsbeeck BG. Dietary fecal tagging as a cleansing method before CT colonography: Initial results-polyp detection and patient acceptance. Radiology 2002; 224(2): 393–403. doi:10.1148/radiol.2241011222 76
97. Thomeer M, Bielen D, Vanbeckevoort D, Dymarkowski S, Gevers A, Rutgeerts P, et al. Patient acceptance for CT colonography: what is the real issue? Eur Radiol 2002; 12(6): 1410–1415. doi:10.1007/s003300101082 76
98. Wan M, Liang ZR, Ke Q, Hong LC, Bitter I, Kaufman A. Automatic centerline extraction for virtual colonoscopy. IEEE Trans Med Imag 2002; 21(12): 1450–1460. doi:10.1109/tmi.2002.806409 76
99. Laghi A, Iannaccone R, Carbone I, Catalano C, Di Giulio E, Schillaci A, Passariello R. Detection of colorectal lesions with virtual computed tomographic colonography. Am J Surg 2002 183(2): 124–131. doi:10.1016/s0002-9610 (01)00857–1 74
100. Shinners TJ, Pickhardt PJ, Taylor AJ, Jones DA, Olsen CH. Patient-controlled room air insufflation versus automated carbon dioxide delivery for CT colonography. Am J Roentgenol 2006; 186(6): 1491–1496. doi:10.2214/ajr.05.0416 73
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Citations per year

Citations per year ranged from 4.5 per year to 84.21 per year with a median of 8.28 citations per year. A list of the top 20 articles with most number of citations per year is given in Table 2.

Table 2.

Top 20 cited CTC articles in descending order of the most number of citations received per year

Rank Article Citations per year
1. Pickhardt PJ, Choi JR, Hwang I, Butler JA, Puckett ML, Hildebrandt HA, et al. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med 2003; 349(23): 2191–2200. doi:10.1056/NEJMoa031618 84.21
3. Johnson CD, Chen MH, Toledano AY, Heiken JP, Dachman A, Kuo MD, et al. Accuracy of CT colonography for detection of large adenomas and cancers. N Engl J Med 2008; 359(12); 1207–1217. doi:10.1056/NEJMoa0800996 55.33
7. Kim DH, Pickhardt PJ, Taylor AJ, Leung WK, Winter TC, Hinshaw JL, et al. CT colonography versus colonoscopy for the detection of advanced neoplasia. N Engl J Med 2007; 357(14); 1403–1412. doi:10.1056/NEJMoa070543 35.4
4. Cotton PB, Durkalski VL, Benoit PC, Palesch YY, Mauldin PD, Hoffman B, et al. Computed tomographic colonography (virtual colonoscopy) - a multicenter comparison with standard colonoscopy for detection of colorectal neoplasia. J Am Med Assoc 2004; 291(14): 1713–1719. doi:10.1001/jama.291.14.1713 34.23
5. Rockey DC, Poulson E, Niedzwiecki D, Davis W, Bosworth HB, Sanders L, et al. Analysis of air contrast barium enema, computed tomographic colonography, and colonoscopy: prospective comparison. Lancet 2005; 365(9456): 305–311. 31.08
2. Fenlon HM, Nunes DP, Schroy PC, Barish MA, Clarke PD, Ferrucci JT. A comparison of virtual and conventional colonoscopy for the detection of colorectal polyps. N Engl J Med 1999; 341(20): 1496–1503. doi,10.1056/nejm199911113412003. 28.61
8. Zalis ME, Barish MA, Choi JR, Dachman AH, Fenlon HM, Ferrucci JT, et al. CT colonography reporting and data system: A consensus proposal. Radiology 2005; 236(1): 3–9. doi:10.1148/radiol.2361041926 26.75
6. Yee J, Akerkar GA, Hung RK, Steinauer-Gebauer AM, Wall SD, McQuaid KR. Colorectal neoplasia, Performance characteristics of CT colonography for detection in 300 patients. Radiology 2001; 219(3): 685–692. 22.5
22. Graser A, Stieber P, Nagel D, Schafer C, Horst D, Becker CR, et al. Comparison of CT colonography, colonoscopy, sigmoidoscopy and faecal occult blood tests for the detection of advanced adenoma in an average risk population. Gut 2009; 58(2); 241–248. doi:10.1136/gut.2008.156448 22.38
57. Stoop EM, de Haan MC, de Wijkerslooth TR, Bossuyt PM, van Ballegooijen M, Nio CY, et al. Participation and yield of colonoscopy versus non-cathartic CT colonography in population-based screening for colorectal cancer: a randomised controlled trial. Lancet Oncol 2012; 13(1): 55–64. doi:10.1016/s1470-2045(11)70283-2 22
54. Pickhardt PJ, Hassan C, Halligan S, Marmo R. Colorectal cancer, CT colonography and colonoscopy for detection-systematic review and meta-analysis. Radiology 2011 259(2): 393–405. doi,10.1148/radiol.11101887 18.83
13. Mulhall BP, Veerappan GR, Jackson JL. Meta-analysis, Computed tomographic colonography. Ann Intern Med 2005 142(8): 635–650. 18.17
15. Halligan S, Altman DG, Taylor SA, Mallett S, Deeks JJ, Bartram CI, Atkin, W. CT colonography in the detection of colorectal polyps and cancer: systematic review meta-analysis and proposed minimum data set for study level reporting. Radiology 2005; 237(3): 893–904. doi:10.1148/radiol.2373050176 17.5
47. Flicek KT, Hara AK, Silva AC, Wu Q, Peter MB, Johnson CD. Reducing the radiation dose for CT colonography using adaptive statistical iterative reconstruction, A pilot study. Am J Roentgenol 2010; 195(1): 126–131. doi:10.2214/ajr.09.3855 17.43
11. Johnson CD, Harmsen WS, Wilson LA, MacCarty RL, Welch TJ, Ilstrup D. M. Prospective blinded evaluation of computed tomographic colonography for screen detection of colorectal polyps. Gastroenterology 2003; 125(2): 311–319. doi:10.1016/s0016-5085 (03)00894–1 17.14
36. Lieberman D, Nadel M, Smith RA, Atkin W, Duggirala SB, Fletcher R, et al. Standardized colonoscopy reporting and data system: report of the Quality Assurance Task Group of the National Colorectal Cancer Roundtable. Gastrointest Endosc 2007; 65(6): 757–766. doi:10.1016/j.gie.2006.12.055 14.6
26. Summers RM, Yao JH, Pickhardt PJ, Franaszek M, Bitter I, Brickman D, et al. Computed tomographic virtual colonoscopy computer-aided polyp detection in a screening population. Gastroenterology 2005; 129(6): 1832–1844. doi:10.1053/j.gastro.2005.08.054 14.42
53. Regge D, Laudi C, Galatola G, Della Monica P, Bonelli L, Angelelli G, et al. Diagnostic accuracy of computed tomographic colonography for the detection of advanced neoplasia in individuals at increased risk of colorectal cancer. J Am Med Assoc 2009; 301(23): 2453–2461. 14.38
20. Iannaccone R, Laghi A, Catalano C, Mangiapane F, Lamazza A, Schillaci A, et al. Computed tomographic colonography without cathartic preparation for the detection of colorectal polyps. Gastroenterology 2004; 127(5): 1300–1311. doi:10.1053/j.gastro.2004.08.025 14.31
9. Fletcher JG, Johnson CD, Welch TJ, MacCarty RL, Ahlquist DA, Reed JE, et al. Optimization of CT colonography technique: Prospective trial in 180 patients. Radiology 2000; 216(3): 704–711. 14.29
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CTC, CT colonography.

Year of publication

These articles were published between 1996 and 2012. The median was found to be 2003. Most of the articles were published in the 2000's. Figure 1 is a graphical representation of the distribution of the top 100 cited articles by a 5year span of publication.

Figure 1.

Figure 1.

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Distribution of the 100 top-cited articles in CTC GI Imaging by 5-year span of publication. CTC, CT colonography; GI, gastrointestinal.

Most common authors and number of authors

The total number of authors for the 100 most-cited works was noted to be 432, not including any research groups listed. Of these 432 authors, 60 had contributed to two articles each and a total of 312 authors had contributed to a single article.

Number of authors listed for any single publication ranged from 1 to 25. Most frequently 6 to 10 (n = 52) authored an article. This was followed by 1–5 (n = 36), 11 to 15 (n = 5) authors and 16 or more authors (n = 7). Mode and median were determined to be six authors. Authors contributed from 1 to 20 articles. Table 3 displays authors who contributed to more than five of the top 100 list. It also indicates these authors total contribution to the field of CTC imaging.

Table 3.

Authors who contributed to more than five of the 100 top-cited articles in CTC GI Imaging

Author # of articles in top 100 Total # of CTC/VC-related publications author has published
Johnson CD 20 67
Pickhardt PJ 13 188
Yee J 11 52
Hara AK 11 24
Maccarty RL 9 19
Halligan S 8 119
Laghi A 8 67
Ahlquist DA 8 25
Reed JE 8 10
Taylor SA 7 89
Harmsen WS 7 16
Welch TJ 7 11
Dachman AH 6 53
Macari M 6 25
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Departmental affiliation

Departmental affiliations of first authors totalled eight different fields and are presented in Table 4. Departmental affiliation was most frequently radiology (n = 81), followed by gastroenterology (n = 9) and internal medicine (n = 6).

Table 4.

Departmental affiliations of authors of the 100 top-cited articles in CTC GI imaging

Departmental affiliation Frequency (n)
Radiology 81
Gastroenterology 9
Internal medicine 6
Oncology 1
Psychiatry 1
Computer science 1
Electrical engineering 1
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Journals

22 journals have published these 100 most-cited articles. A list of top journals including impact factor is given in Table 5. The remainder of the journals published one article each of the most-cited works.

Table 5.

Journals in which the 100 top-cited articles in CTC GI imaging were published

Journal Frequency (n) Impact factor
Radiology 37 6.867
American Journal of Roentgenology 19 2.73
Gastroenterology 10 16.716
IEEE Transactions on Medical Imaging 5 3.39
New England Journal of Medicine 4 55.873
American Journal of Gastroenterology 4 10.755
European Radiology 4 4.014
Gastrointestinal Endoscopy 3 5.369
JAMA - Journal of the American Medical Association 2 35.289
GUT 2 14.660
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Design and analyses

Study design was primarily prospective (n = 57), followed by retrospective (n = 28) and randomized controlled trials (n = 5). The remaining 10 papers were reviews. These results are displayed in Table 6. Statistical analysis was done in 86 of these articles. Of the 14 without analyses done, 6 were retrospective studies, 4 were reviews and 4 were prospective.

Table 6.

Study design of 100 top-cited articles in CTC GI imaging

Study design Frequency (n)
Prospective 57
Retrospective 28
Review paper 10
Randomized controlled trial 5
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Sample size

Sample size, or human patient numbers for the articles is presented in Figure 2. Median sample size was 165. Sample size was not stated for 15 articles.

Figure 2.

Figure 2.

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Sample size of the 100 top-cited articles in CTC GI imaging.

Country of origin

Most of the papers were published from the USA (n = 72), followed by Italy (n = 7) and England (n = 7). The results are displayed in entirety below in Table 7.

Table 7.

Country of first author for 100 top-cited articles in CTC GI imaging

Country of first author Frequency (n)
USA 72
Italy 8
England 7
Belgium 4
Netherlands 4
Sweden 2
Germany 1
Israel 1
Switzerland 1
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Number of institutions

Number of affiliated institutions with each publication ranged from 1 to 19. Most frequently one (n = 51) or two (n = 21) institutions were listed. These results are displayed in more detail in Table 8. Of the top 100 articles, 77 were affiliated with more than one department and 21 were affiliated with more than one hospital.

Table 8.

Number of affiliated institutions per paper of 100 top-cited articles in CTC GI imaging

Number of affiliated institutions per paper Frequency (n)
1 51
2 21
3–5 19
6–10 3
>10 6
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Topics

Each article was evaluated for its primary topic/objective. Of these 100 most-cited CTC articles, 40 focused on CTC imaging technique and 28 covered diagnostic utility of an imaging modality (comparison with another modality, sensitivity/specificity/PPV/NPV). Clinical uses of CTC were covered in 18 articles. Patient preference and perception of CTC was covered in seven papers, economic impact/cost-effective analyses of CTC as a screening tool was covered in five papers and two articles covered multiple topics.

Discussion

Our analysis revealed that the most-cited article in CTC is the 2003 paper by Pickhardt et al “Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults,” published in The New England Journal of Medicine. It was also the article with the most citations per year since publication, with 84.21 average citations per year. 63 of the 100 most-cited articles were published before 2005, biasing the list in favour of articles that have had longer periods of time since publication to accumulate citations. Therefore, we also included the measure of citations per year. The advantage of using citations per year is that it corrects the total citations for time since publication.

Careful interrogation of the content of top articles brought forth several noteworthy findings, i.e. we noted that of the top three articles, which are garnering the most citations per year, two are related to diagnostic outcomes and one is in regard to screening (Table 1). We feel that this could be because in modern medicine, there is more interest in sensible application of imaging and maximizing detection rates.21,22 Three articles described the significantly lower risk of severe complications, specifically perforation, during CTC when compared with optical colonoscopy. The works determined that the risk approached 0% in CTC. Old age and concomitant colorectal disease were noted to represent risk factors for perforation. Five articles demonstrate the distinct advantage of using CTC to detect clinically significant extracolonic findings such as abdominal aortic artery aneurysms or extracolonic malignancies. The average additional cost per patient ranged from $28 to $34. This point seemed quite contentious as the economic impact of these additional findings and subsequent investigations and/or management was unknown but CTC is still thought to be the safest and most cost-effective screening method especially with non-reporting of diminutive lesions and considering its ability to detect extracolonic findings.

The journal with the most publications was Radiology at 37. American Journal of Roentgenology was second with 19. Both journals reach a great number of medical practitioners, in particular radiologists. Behind these two journals was Gastroenterology with 10 articles. No other journals contributed more than five journals to the 100 most-cited list. This pattern of only a few journals predominating the top 100 citations is consistent with previously compiled bibliometric analyses.5,11,14–18 To our surprise, 25% of the top 100 articles had a sample size stated of less than or equal to 50. This could have significant impact for future studies in CTC, as it could imply that having a large sample size is not necessary to have an impactful study, or it could imply that early, novel, small studies get cited a lot because they are first to report new data.

Upon analysing the yearly distribution of the most-cited CTC articles by topic, a few temporal trends were noted (Figure 3). The early years of CTC saw an abundance of articles describing technique, including dose optimization, patient preparation and positioning, image reconstruction and use of computer-aided detection. This then gave way to studies that compared CTC with established screening and imaging methods as well as the reliability and reproducibility of its results. This coincided with publications that analysed patients’ perception and preference towards CTC. Following this, studies focused more on the clinical utility and implementation of CTC as well as establishing the best use-case scenarios and development of a standardized reporting system. Finally, papers analysing the cost-effectiveness of CTC and the economic impact of this new modality began to appear, albeit in limited numbers. These trends generally follow what is expected when a new technique or technology is introduced from inception to dissemination and wide-spread adoption. Of note, studies which compared CTC with another imaging modality were the most regularly published throughout both early and late years of our analysis (1995–2013). We believe that this is the first bibliometric analysis focusing on CTC. Having a focused list can help radiologists and scientists by providing an accessible list of the most influential articles in CTC. The subspecialty analysis done also allows for a better understanding of what a highly cited work consists of, and where future research interests may lie. Understanding the composition of highly cited subspecialty works also allows editors and reviewers to evaluate unpublished articles. Niche bibliometric analysis such as ours in this paper has a stronger direct impact than general radiology lists, as most of radiology journals are subspecialty focused.

Figure 3.

Figure 3.

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Yearly distribution of most-cited CTC articles by topic. CTC, CT colonography.

We noted that a large portion of prior bibliometric analysis done in radiology restricted their searches to only include radiology journals. As the role of radiology in patient-care grows, we felt that this was a significant limitation that excludes many relevant scientific journals. Radiology is intertwined in so many fields such as emergency medicine, trauma surgery, orthopedics, etc. which makes us feel that literature in those fields could be extremely relevant and important. This opinion prompted us to investigate the impact of works published in non-radiology journals on our analysis.

We established that 31% of the 100 top-cited CTC articles were published in non-radiology journals and 19% of the first authors had a departmental affiliation other than radiology. Studies that demonstrated that CTC was inferior to optical colonoscopy were exclusive to non-radiology journals. None of the journals that published cost-benefit analysis were radiology specific. Five of the highest cited papers on CTC discussed the economic impact of CTC, taking into consideration the additional extracolonic findings. Two of the five articles favoured economic savings over time by employing CTC as a screening modality, whereas two others predicted an increase in overall cost by utilizing CTC as a screening modality. One article remained neutral and suggested further investigation into the matter. Finally, both the top three cited papers, and the top-cited papers per year were published in the New England Journal of Medicine, not a radiology specific journal (Tables 1 and 2). The intertwined nature of radiology in modern medicine cannot be understated, and for this reason we strongly recommend that future studies, which focus on bibliometrics in radiology should expand their inclusion criteria to include non-radiology journals.

Limitations

We are aware that our study being a bibliometric analysis by nature has limitations. The main limitation is the search terms, which were used to create the database. To be more specific, articles that did not use the term “gastrointestinal” did not appear in our database collection. We did not use the term “gut” instead of “gastrointestinal” because it created a wide-ranging list, which failed to capture many articles in our database. Similarly, our results were restricted to articles, which included “CTC”. As in other bibliometric analysis, we are aware that our list of articles is limited by the accuracy and inclusiveness of the keywords identified by the database.3

Citation counts from databases such as WOS, Scopus, Pubmed and Google Scholar often differ.2,5,16,17 We decided to use citation counts from WOS because we felt it was the most precise and accommodating with our search terms. One problem bibliometric analysis often face is that of the bias in favour of older publications.2 For this reason, we included the measure of citations per year to better identify publications with the most impact. Lastly, we found that our results had several articles which did not meet our final inclusion criteria, so we had two attending radiologists independently confirm article applicability.

Conclusion

Bibliometric analysis in academic medicine has enormous potential for future growth. Our study provides intellectual milestones in CTC research, reflecting on the characteristics and quality of published literature. Focused bibliometric analyses reveal characteristics of highly cited works. This information has implications for clinical radiologists, scientists, researchers and editors. Bibliometric analyses appraise us of the most influential articles of the current time and allow us to predict future trends in medical subspecialties.

Disclosure

Faisal Khosa is the American Roentgen Ray Society Scholar (2013–2016). No financial disclosures or conflict of interest on behalf of the authors. There was no commercial funding for this study.

Contributor Information

Mohammed Fahim Mohammed, Email: mohammed.f.mohammed@gmail.com.

Tejbir Chahal, Email: tejbirschahal@gmail.com.

Bo Gong, Email: bogong.ustc@gmail.com.

Nizar Bhulani, Email: nizar.bhulani@gmail.com.

Michael O’Keefe, Email: dr.meokeeffe@gmail.com.

Timothy O’Connell, Email: timothy.oconnell@vch.ca.

Savvas Nicolaou, Email: Savvas.Nicolaou@vch.ca.

Faisal Khosa, Email: Faisal.Khosa@vch.ca.

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