Abstract
Background
This article provides surgical trainees with a ranked list of the foundational literature that guides the contemporary surgical management of colorectal cancer and shows the evolution of surgical techniques in the field.
Methods
We assessed the surgical literature using the Web of Science and other ranking systems to create a ranked list of published articles on colorectal cancer surgery.
Results
We compiled a ranked list of the top 25 articles in the surgical management of colorectal cancer, based on the citation density score (mean number of citations per year) and the individual author H-index. The mean density score of the 25 papers was 29.9, and the journal most frequently represented on our list was the Annals of Surgery (36% of top papers). The Web of Science (primary) and alternative databases (secondary) H-index values for each author were identified. The range, mean, and median of the primary H-index values were 7.0–84.0, 31.8, and 29.0, respectively. The range, mean, and median of secondary H-index values were 4.0–108.0, 48.6, and 45.0, respectively. A 2-tailed, unpaired t-test was used to determine whether a significant difference existed between the primary and secondary H-index values for primary authors; P = .0376 (95% confidence interval, 1.02–32.58). A citation density score was calculated for each article, which represented the mean number of citations per year.
Conclusion
We provided a ranked list (citation density score) of the top-cited 25 articles in colorectal cancer surgery, a ranking of the associated primary authors by H-index, and a comparison of H-index scores between primary and secondary database sources. We believe this list is a useful resource for surgical trainees and researchers in colorectal cancer field and provides easy access to the top papers in this discipline.
Keywords: colorectal cancer, colorectal neoplasms, rectal neoplasms, surgical oncology, surgical trainees, h-index, journal impact factor, bibliometrics
Introduction
The advancement of the Information Age, which has evolved into the Intelligence Age, provides the learner with straightforward and fast access to digital scientific literature.1 Medical students and residents can now consult peer-reviewed research on mobile devices or tablets, which has the benefit of rapidly expanding their knowledge repository and access to information. Furthermore, information can be shared easily and quickly using commonly available communication applications. However, the ease of access and rapid transmission have also created a larger volume of available information, making it difficult for trainees to identify high-quality sources of greatest impact and value for advancing their knowledge.
Peer-reviewed evidence-based research is the main modality by which surgeons steer modern-day surgical management for colorectal cancer. This management requires a multi-disciplinary approach involving intricate treatment algorithms. Society guidelines are based on this research and serve as clinical reference tools to aid the surgeon, but it is necessary to understand the foundational literature and tailor that knowledge to a patient-specific approach. With an ever-increasing patient census, this can represent a daunting task. Furthermore, numerous studies have predicted a shortage of surgeons available to provide care to the growing population in the United States,2 and suggest an overall increase in workforce deficits in the setting of growing clinical demands.3
Since the start of the 20th century, the approach to the treatment of colorectal cancer has shifted from radical surgical procedures to a more targeted, nuanced, and multi-disciplinary approach. In the 21st century, the field of colorectal surgery continues to evolve. In this report, we sought to rank the top 25 peer-reviewed papers to guide the contemporary surgical management of colorectal cancer. While studies have attempted to offer similar summation of colorectal research, there has not been a similar review completed since 2021.4 Additionally, that most recent article focused on rectal cancer alone. Our goal was to establish an easily accessible, metric-based resource for learners to identify the most influential articles in the field of both colon and rectal cancer.
Methods
We queried the Web of Science Citation Index in October 2024 using guidance from a previously published work.5 The Web of Science search engine is a subscription-based platform that utilizes multiple databases to compile citation data from academic journals across several scientific disciplines. Our search period was limited to 26 years (January 1, 1998, to October 1, 2024). The terms “colon cancer” and “rectal cancer” were input into the citation reference search area. Results were restricted to journal articles written in the English language. Only those articles tagged with “surgery,” “oncology,” “general internal medicine,” and “gastroenterology and hepatology” within the Web of Science categories list were considered.
We created a ranked list of publications arranged in descending order by total number of citations. A citation density score was also calculated, which represented the mean number of citations per year for an individual article. Finally, the overall number of citations associated with the article were listed. Consensus statements, society guidelines, and other works not considered primary research were excluded. Articles deemed irrelevant (eg, due to a focus outside the area of surgical management for colorectal cancer) were excluded, with any discrepancies resolved by 2 independent, colorectal surgeons before inclusion in our list. The final list of publications was rearranged in descending order using their citation density score.
The H-index is widely regarded as a surrogate for an author’s impact on any given field; however, there is no agreed upon repository for these values for any specific author because this value is database specific and can vary. This makes the H-index for an author variable, determined by which database an investigator has access to. For this reason, the H-index for the authors listed in these articles were derived from the Web of Science database as well as Google Scholar for the purpose of comparison (the National Library of Medicine’s database, PubMed, was excluded because it does not record article citation counts and therefore is unable to calculate an H-index value for any given author).
Inconsistencies between databases, the number of reported citations, and the individual author H-indices, have long been known to exist.6 The H-index for each primary author was identified via the Web of Science Database and recorded as the primary H-index value. The H-index for each primary author was cross-referenced against the H-index reported on both Google Scholar and Research Gate. We used the higher H-index from these 2 resources and recorded it as the secondary H-index value. If an author was listed as primary for more than 1 article, they were included only once in the statistical calculations. We employed a 2-tailed, unpaired t-test to determine if there was a significant mean difference between the 2 sources of H-index values.
Results
Our search yielded more than 25 000 articles with the top 25 articles displayed in order of citation density score (Table 1 and Table 2). The total number of citations among the 25 articles was 14 511 (mean 580.4 ± 304), with a range of 322 to 1349. The mean density score was 29.9 ± 17.0.
Table 1.
Top 25 Articles, Based on Citation Density, in the Surgical Management of Colorectal Cancer
| Rank | Publication information | Total citations | Density score |
|---|---|---|---|
| 1 | Standardized surgery for colonic cancer: complete mesocolic excision and central ligation - technical notes and outcome Authors: Hohenberger, W; Weber, K; Matzel, K; Papadopoulos, T; Merkel, S Source: Colorectal Disease Published: May, 2009 PMID: 19016817 |
1160 | 72.5 |
| 2 | Operative versus nonoperative treatment for stage 0 distal rectal cancer following chemoradiation therapy - Long-term results Authors: Habr-Gama, A; Perez, RO; Nadalin, W; Sabbaga, J; Ribeiro, U; Sousa, AHSE; Campos, FG; Kiss, DR; Gama-Rodrigues, J Source: Annals of Surgery Published: October, 2004 PMID: 15383798 |
1349 | 64.2 |
| 3 | The TME trial after a median follow-up of 6 years - Increased local control but no survival benefit in irradiated patients with resectable rectal carcinoma Authors: Peeters, KCMJ; Marijnen, CAM; Nagtegaal, ID; Kranenbarg, EK; Putter, H; Wiggers, T; Rutten, H; Pahlman, L; Glimelius, B; Leer, JW; van de Velde, CJH Source: Annals of Surgery Published: November, 2007 PMID: 17968156 |
914 | 50.9 |
| 4 | Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer Authors: Jayne, DG; Thorpe, HC; Copeland, J; Quirke, P; Brown, JM; Guillou, PJ Source: British Journal of Surgery Published: November, 2010 PMID: 20629110 |
762 | 50.8 |
| 5 | Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group Trial Authors: Fleshman, J; Sargent, DJ; Green, E; Anvari, M; Stryker, SJ; Beart, RW; Hellinger, M; Flanagan, R; Peters, W; Nelson, H Source: Annals of Surgery Published: October, 2007 PMID: 17893502 |
876 | 48.7 |
| 6 | Long-term results of a randomized trial comparing preoperative short-course radiotherapy with preoperative conventionally fractionated chemoradiation for rectal cancer Authors: Bujko, K; Nowacki, MP; Nasierowska-Guttmejer, A; Michalski, W; Bebenek, M; Kryj, M Source: British Journal of Surgery Published: October, 2006 PMID: 16983741 |
917 | 48.3 |
| 7 | Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer Authors: Green, BL; Marshall, HC; Collinson, F; Quirke, P; Guillou, P; Jayne, DG; Brown, JM Source: British Journal of Surgery Published: January, 2013 PMID: 23132548 |
502 | 41.8 |
| 8 | Rectal cancer - The Basingstoke experience of total mesorectal excision, 1978–1997 Authors: Heald, RJ; Moran, BJ; Ryall, RDH; Sexton, R; MacFarlane, JK Source: Archives of Surgery Published: August, 1998 PMID: 9711965 |
1108 | 41.0 |
| 9 | The long-term results of a randomized clinical trial of laparoscopy-assisted versus open surgery for colon cancer Authors: Lacy, AM; Delgado, S; Castells, A; Prins, HA; Arroyo, V; Ibarzabal, A; Pique, JM Source: Annals of Surgery Published: July, 2008 PMID: 18580199 |
467 | 27.5 |
| 10 | Circumferential margin involvement is still an important predictor of local recurrence in rectal carcinoma - Not one millimeter but two millimeters is the limit Authors: Nagtegaal, ID; Marijnen, CAA; Kranenbarg, EK; van de Velde, CJH; van Krieken, JHJM Source: American Journal of Surgical Pathology Published: March, 2002 PMID: 11859207 |
583 | 25.4 |
| 11 | Risk of lymph node metastasis in T1 carcinoma of the colon and rectum Authors: Nascimbeni, R; Burgart, LJ; Nivatvongs, S; Larson, DR Source: Diseases of the Colon and Rectum Published: February, 2002 PMID: 11852333 |
536 | 23.3 |
| 12 | The prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined Authors: Swanson, RS; Compton, CC; Stewart, AK; Bland, KI Source: Annals of Surgical Oncology Published: January–February, 2003 PMID: 12513963 |
502 | 22.3 |
| 13 | Prognostic significance of the circumferential resection margin following total mesorectal excision for rectal cancer Authors: Wibe, A; Rendedal, PR; Svensson, E; Norstein, J; Eide, TJ; Myrvold, HE; Soreide, O Source: British Journal of Surgery Published: March, 2002 PMID: 11872058 |
504 | 21.9 |
| 14 | Rates of circumferential resection margin involvement vary between surgeons and predict outcomes in rectal cancer surgery Authors: Birbeck, KF; Macklin, CP; Tiffin, NJ; Parsons, W; Dixon, MF; Mapstone, NP; Abbott, CR; Scott, N; Finan, PJ; Johnston, D; Quirke, P Source: Annals of Surgery Published: April, 2002 PMID: 11923599 |
503 | 21.8 |
| 15 | Robotic versus laparoscopic low anterior resection of rectal cancer: short-term outcome of a prospective comparative study Authors: Baik, SH; Kwon, HY; Kim, JS; Hur, H; Sohn, SK; Cho, CH; Kim, H Source: Annals of Surgical Oncology Published: June, 2009 PMID: 19290486 |
335 | 20.9 |
| 16 | Randomized clinical trial comparing laparoscopic and open surgery in patients with rectal cancer Authors: Lujan, J; Valero, G; Hernandez, Q; Sanchez, A; Frutos, MD; Parrilla, P Source: British Journal of Surgery Published: September, 2009 PMID: 19644973 |
320 | 20.0 |
| 17 | A prospective, randomized trial comparing laparoscopic versus conventional techniques in colorectal cancer surgery: A preliminary report Authors: Milsom, JW; Bohm, B; Hammerhofer, KA; Fazio, V; Steiger, E; Elson, P Source: Journal of the American College of Surgeons Published: July, 1998 PMID: 9660024 |
502 | 18.6 |
| 18 | More extensive nodal dissection improves survival for stages I to III of colon cancer - a population-based study Authors: Chen, SL; Bilchik, AJ Source: Annals of Surgery Published: October, 2006 PMID: 16998369 |
346 | 18.2 |
| 19 | Anterior resection for rectal cancer with mesorectal excision - a prospective evaluation of 622 patients Authors: Law, WL; Chu, KW Source: Annals of Surgery Published: August, 2004 PMID: 15273550 |
364 | 17.3 |
| 20 | The modern abdominoperineal excision - The next challenge after total mesorectal excision Authors: Marr, R; Birbeck, K; Garvican, J; Macklin, CP; Tiffin, NJ; Parsons, WJ; Dixon, MF; Mapstone, NP; Sebag-Montefiore, D; Scott, N; Johnston, D; Sagar, P; Finan, P; Quirke, P Source: Annals of Surgery Published: July, 2005 PMID: 15973104 |
332 | 16.6 |
| 21 | Oncological outcomes after total mesorectal excision for cure for cancer of the lower rectum: Anterior vs. abdominoperineal resection Authors: Wibe, A; Syse, A; Andersen, E; Tretli, S; Myrvold, HE; Soreide, O Source: Diseases of the Colon and Rectum Published: January, 2004 PMID: 14719151 |
344 | 16.5 |
| 22 | Long-term oncologic outcome following preoperative combined modality therapy and total mesorectal excision of locally advanced rectal cancer Authors: Guillem, JG; Chessin, DB; Cohen, AM; Shia, J; Mazumdar, M; Enker, W; Paty, PB; Weiser, MR; Klimstra, D; Saltz, L; Minsky, BD; Wong, WD Source: Annals of Surgery Published: May, 2005 PMID: 15849519 |
327 | 16.4 |
| 23 | Laparoscopic total mesorectal excision (TME) for rectal cancer surgery - long-term outcomes Authors: Leroy, J; Jamali, F; Forbes, L; Smith, M; Rubino, F; Mutter, D; Marescaux, J Source: Surgical Endoscopy and Other Interventional Techniques Published: February, 2004 PMID: 14691716 |
310 | 14.8 |
| 24 | A pathologic complete response to preoperative chemoradiation is associated with lower local recurrence and improved survival in rectal cancer patients treated by mesorectal excision Authors: Garcia-Aguilar, J; de Anda, EH; Sirivongs, P; Lee, SH; Madoff, RD; Rothenberger, DA Source: Diseases of the Colon & Rectum Published: March, 2003 PMID: 12626903 |
322 | 14.6 |
| 25 | Is local excision adequate therapy for early rectal cancer? Authors: Mellgren, A; Sirivongs, P; Rothenberger, DA; Madoff, RD; Garcia-Aguilar, J Source: Diseases of the Colon and Rectum Published: August, 2000 PMID: 10950004 |
326 | 13.0 |
Abbreviations: TME = total mesorectal excision; CLASICC = conventional versus laparoscopic-assisted surgery in colorectal cancer; COST = clinical outcomes of surgical therapy; PMID = PubMed index number
Table 2.
H-Index Values for the Primary Author of Papers Ranked by Density Score
| Rank | PMID | H-Index (1°) | H-Index (2°) |
|---|---|---|---|
| 1 | 19016817 | 40 | 11 |
| 2 | 15383798 | 37 | 63 |
| 3 | 17968156 | 16 | * |
| 4 | 20629110 | 84 | 59 |
| 5 | 17893502 | 35 | 82 |
| 6 | 16983741 | 25 | 34 |
| 7 | 23132548 | 17 | * |
| 8 | 9711965 | 18 | * |
| 9 | 18580199 | 29 | 51 |
| 10 | 11859207 | 59 | 95 |
| 11 | 11852333 | 15 | 28 |
| 12 | 12513963 | * | 24 |
| **13 | 11872058 | 17 | 40 |
| 14 | 11923599 | 7 | 7 |
| 15 | 19290486 | 36 | 45 |
| 16 | 19644973 | * | 40 |
| 17 | 9660024 | 24 | 62 |
| 18 | 16998369 | 29 | * |
| 19 | 15273550 | 32 | 45 |
| 20 | 15973104 | * | 4 |
| **21 | 14719151 | 17 | 40 |
| 22 | 15849519 | 46 | 108 |
| 23 | 14691716 | 23 | * |
| 24 | 12626903 | 53 | 75 |
| 25 | 10950004 | 26 | 51 |
n/a denotes unavailability of H-index from the identified source
the primary author listed for articles number 13 and 21 was the same
Abbreviation: PMID = PubMed index number
We counted the journal names in the list and found the Annals of Surgery (36%) had the highest number of papers followed by the British Journal of Surgery (20%) and Diseases of the Colon and Rectum (16%).
The primary H-index value range, mean, and median values were 7.0–84, 31.8, and 29.0, respectively. The secondary H-index value range, mean, and median values were 4.0–108, 48.6, and 45.0, respectively. The 2-tailed, unpaired Student’s t-test revealed a significant difference between the primary and secondary H-index values of the primary authors (P = .0376, 95% confidence interval; 1.02–32.58).
Discussion
The management of colorectal cancer has advanced significantly over the past century and continues to evolve.7 Modern-day management of colorectal cancer is multidisciplinary in approach. Aside from the surgical aspect, many studies have contributed to the sophisticated and highly intricate methodology of the modern-day approach to the treatment of colorectal cancer. Advances in chemotherapeutic regimens such as those reported in the MOSAIC and IDEA trials continue to lay the groundwork for contemporary chemotherapy treatments for colorectal cancer.8,9 Progression in radiotherapy techniques combined with a total neoadjuvant therapeutic approach, such as those reported by the RAPIDO and PRODIGE-23 trials, have led to improvements in disease-free survival.9,10 The impact of these developments in chemoradiation therapy has been astounding, such that a “Watch and Wait” approach is now a viable option for select patients.11,12 With trials like the OPRA trial reporting no difference in disease-free survival, the potential for sparing patients major surgery and its associated morbidities is now a realistic option.13 Indeed, improvements in the management of metastatic disease using chemotherapeutic regimens and monoclonal antibodies as conversion therapy (CELIM, VOLFI, OPTILIV trials) have contributed to an increase in disease-free survival.14–16 In select patients, these regimens are potentially curative when combined with surgery.
With the increasing number of advancements made in the surgical management of colorectal cancer17–20 and the growing number of associated publications, it can be difficult for surgical trainees to identify impactful sources. The surgical management of colorectal cancer is very detailed, and surgical trainees face several challenges throughout their training integrating these details.21 An additional challenge includes interpretation of the literature, and often involves an aspect of information overload, information fragmentation, rapid changes with conflicting evidence, limited time for thorough evaluation, and a lack of proper authoritative guidance. We completed an analysis of existing literature in colorectal cancer surgery, compiled a list of top-ranked papers, and compared the H-index of the primary authors from different available indexes. Our list can be used to quickly access the most frequently cited papers in a rapidly evolving field.
There are several metrics that can be used to calculate the academic value of a single author’s contribution to the academy. One metric is the H-index, which is commonly used and regarded as one of the main ranking systems for an author’s impact in their given field22 and is also a factor in academic promotion among surgeons.23 The H-index is derived from an author’s number of publications and the number of citations an author’s work has received. For an author to have a high H-index, an author must have a large number of publications that have been cited multiple times. Because the H-index discounts the disproportionate weight of highly cited publications as well as work that has not yet been published, it is widely regarded as a durable representative of the impact an author has on their chosen specialty.
The Web of Science was the first database to include the H-index, and indexes over 10 000 journals.24 The H-index value regarded as average, good, or excellent remains up for debate; however, an H-index greater than 30 is generally considered excellent.21 We found H-indexes ranging from 7 to 108 suggesting that our list of 25 publications included the work of accomplished authors, providing value to the surgical trainee. In addition, the associated authors appeared to provide topics of significant relevance to the field of colorectal surgery. Of note, the significant level of variability among the H-indices when compared between 2 of the most commonly used databases (Web of Science and Google Scholar) is noteworthy (P = .0376, 95% CI; 1.02–32.58). This variability is interesting to observe when considering an author and their article’s impact in the field of colorectal surgery and further serves to highlight the inherent discrepancies between individual databases.
Overall, evidence-based medicine is grounded in randomized controlled trials with large sample sizes that control for confounding variables. The importance of a study’s findings is further strengthened by its reproducibility and incorporation into treatment algorithms and guidelines. However, the precise influence an article has on its respective field can be difficult to quantify. Nevertheless, the number and frequency of citations can be a surrogate for a paper’s impact. In the absence of a defined metric for influence, we believe the number of citations and citation density identifying the top papers provides a good representation of pertinent literature for surgical trainees and attending surgeons. Stegall et al published a paper on the most influential articles published in vascular surgery.5 Our work parallels their work and fills a gap for information in the colorectal cancer surgery realm. Other articles ranking publications regarding the management of multiple colorectal pathologies have been published, but these are either too broad or don’t address the surgical management of colorectal cancer specifically.25,26 Therefore, our paper fills a need by providing a concise list of recent work in the field.
We identified several limitations in our work, the most significant being database restrictions. Despite a large number of journals queried within the Web of Science citation search index, the results are not all-inclusive. H-indices are database specific and will be derived only from an author’s published work within that database. If 2 databases have identical publications for an author, both of these databases will have the same author-specific H-index. However, if 1 database does not contain the same publications as another database for a given author, then there will be variation in the author’s H-index as is shown in Table 2 with a comparison of the primary and secondary H-index values. Because the coverage between databases varies, no single resource can provide a comprehensive measurement of a given author’s impact. Another limitation is that we were unable to account for authors self-citing. This practice would contribute to the overall citation number and frequency of citations.27 Finally, we presented these top 25 articles with the assumption that the citations associated with these reports were for a positive portrayal. That is to say, the many citations associated with these articles are being used to illustrate progressive ideas within the field of colorectal surgery, and not maladaptive concepts or unfounded hypotheses.
Conclusion
The future management of colorectal cancer is an exciting and rapidly evolving field. New developments and understanding disease processes have led to many foundational studies and advancements in the recent past. We believe our report provides a concise list of peer-reviewed foundational literature for surgical trainees in the contemporary surgical management of colorectal cancer. Review of these articles can help surgical trainees establish a strong understanding of not only the past and present of colorectal cancer management but also help to understand future directions.
Acknowledgments
Thank you to Michael G Flynn, PhD, Medical Writer, who provided writing and copyediting assistance on the final version of the manuscript.
Funding Statement
This research was supported (in whole or in part) by HCA Healthcare and/or an HCA Healthcare-affiliated entity.
Footnotes
Conflicts of Interest: The authors declare they have no conflicts of interest.
Dr Schlussel is an employee of HCA Florida Jacksonville Surgical Specialists, a hospital associated with this journal's publisher.
This research was supported (in whole or in part) by HCA Healthcare and/or an HCA Healthcare-affiliated entity. The views expressed in this publication represent those of the author(s) and do not necessarily represent the official views of HCA Healthcare or any of its affiliated entities.
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