PreprintCited by 3Colorectal Cancer Surgical TreatmentsColorectal Cancer Screening and DetectionGastric Cancer Management and Outcomes

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

The effect of preoperative endoscopic tattooing on lymph node retrieval in colorectal cancer: a systematic review and meta-analysis

Open access
Nawras, Mohamad, Chawla, Karan, DeRiso, Armelle, Dubchuk, Christina, Beran, Azizullah, Aziz, Muhammad, Pannell, Stephanie·2023·International Journal of Colorectal Disease

Preprint — published as 10.1007/s00384-023-04466-x · Paper page

Abstract

Purpose The effect of preoperative endoscopic tattooing (ET) on accurate colorectal cancer localization and resection has been well established. However, its effect on lymph node (LN) retrieval remains unclear. The purpose of this study was to systematically compare LN retrieval between patients with colorectal cancer who underwent preoperative ET and those who did not. Methods A systematic search for relevant studies was conducted using the following databases: PubMed, Embase, and Web of Science. Studies that compared LN retrieval in patients with colorectal cancer with and without preoperative ET were included. Weighted pooled odds ratio (OR) and mean difference (MD) with the corresponding 95% confidence intervals (CIs) for all outcomes using the random-effects model were calculated. Results 10 studies, including 2231 patients with colorectal cancer were included. Six studies reported total LN yield and showed significantly higher LN yield in the tattooed group (MD:2.61; 95% CI:1.01–4.21, P = 0.001). Seven studies reported the number of patients with adequate LN retrieval and showed a significantly higher number of patients with adequate LN retrieval in the tattooed group (OR:1.89, 95% CI:1.08–3.32, P = 0.03). However, subgroup analysis revealed that both outcomes were only statistically significant in patients with rectal cancer, and not in patients with colon cancer. Conclusions Our results suggest that preoperative ET is associated with increased LN retrieval in patients with rectal cancer, but not in colon cancer. Further large-scale randomized control trials are necessary to validate our findings.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.21203/rs.3.rs-2958467/v1

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 34

  1. Xi Y, Xu P. Global colorectal cancer burden in 2020 and projections to 2040. Transl Oncol. Oct 2021;14(10):101174. doi:10.1016/j.tranon.2021.101174 · DOI
  2. Vogel JD, Eskicioglu C, Weiser MR, Feingold DL, Steele SR. The American Society of Colon and Rectal Surgeons Clinical Practice Guidelines for the Treatment of Colon Cancer. Dis Colon Rectum. Oct 2017;60(10):999–1017. doi:10.1097/dcr.0000000000000926 · DOI
  3. Feingold DL, Addona T, Forde KA, et al. Safety and reliability of tattooing colorectal neoplasms prior to laparoscopic resection. J Gastrointest Surg. Jul-Aug 2004;8(5):543–6. doi:10.1016/j.gassur.2003.12.016 · DOI
  4. Beretvas RI, Ponsky J. Endoscopic marking: an adjunct to laparoscopic gastrointestinal surgery. Surg Endosc. Oct 2001;15(10):1202–3. doi:10.1007/s004640000304 · DOI
  5. Yeung JM, Maxwell-Armstrong C, Acheson AG. Colonic tattooing in laparoscopic surgery - making the mark? Colorectal Dis. Jun 2009;11(5):527–30. doi:10.1111/j.1463-1318.2008.01706.x · DOI
  6. Onitilo AA, Stankowski RV, Engel JM, Doi SA. Adequate lymph node recovery improves survival in colorectal cancer patients. J Surg Oncol. Jun 2013;107(8):828–34. doi:10.1002/jso.23332 · DOI
  7. Roberto S, Piergiorgio D, Antonio ZM. Lymph node staging for colorectal cancer: Green is the new black. Dig Liver Dis. Dec 2020;52(12):1379–1380. doi:10.1016/j.dld.2020.09.028 · DOI
  8. Le Voyer TE, Sigurdson ER, Hanlon AL, et al. Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089. J Clin Oncol. Aug 1 2003;21(15):2912–9. doi:10.1200/jco.2003.05.062 · DOI
  9. Kelder W, Inberg B, Schaapveld M, et al. Impact of the number of histologically examined lymph nodes on prognosis in colon cancer: a population-based study in the Netherlands. Dis Colon Rectum. Feb 2009;52(2):260–7. doi:10.1007/DCR.0b013e3181979164 · DOI
  10. Xiao WW, Zhang LN, You KY, et al. The total number of lymph nodes harvested from pathological T3N0 rectal cancer patients: Prognostic significance and potential indication for postoperative radiotherapy. J Cancer Res Ther. Jun 2018;14(Supplement):S288-s294. doi:10.4103/0973-1482.235343 · DOI
  11. Chen SL, Bilchik AJ. More extensive nodal dissection improves survival for stages I to III of colon cancer: a population-based study. Ann Surg. Oct 2006;244(4):602–10. doi:10.1097/01.sla.0000237655.11717.50 · DOI
  12. Dawson K, Wiebusch A, Thirlby RC. Preoperative tattooing and improved lymph node retrieval rates from colectomy specimens in patients with colorectal cancers. Arch Surg. Sep 2010;145(9):826–30. doi:10.1001/archsurg.2010.180 · DOI
  13. Nelson BM. Sentinel lymph node biopsies in cancers of the skin, colon, head and neck, and breast. Proc (Bayl Univ Med Cent). Apr 2004;17(2):99–103. doi:10.1080/08998280.2004.11927962 · DOI
  14. Bartels SA, van der Zaag ES, Dekker E, Buskens CJ, Bemelman WA. The effect of colonoscopic tattooing on lymph node retrieval and sentinel lymph node mapping. Gastrointest Endosc. Oct 2012;76(4):793–800. doi:10.1016/j.gie.2012.05.005 · DOI
  15. Wlodarczyk J, Dewberry S, Yoon D, et al. Assessing the Association Between Endoscopic Tattooing and Lymph Node Yield in Rectal Cancer. J Surg Res. Jan 2023;281:37–44. doi:10.1016/j.jss.2022.08.013 · DOI
  16. Goo JJ, Ryu DG, Kim HW, et al. Efficacy of preoperative colonoscopic tattooing with indocyanine green on lymph node harvest and factors associated with inadequate lymph node harvest in colorectal cancer. Scand J Gastroenterol. May 2019;54(5):666–672. doi:10.1080/00365521.2019.1612940 · DOI
  17. Yang M, Pepe D, Schlachta CM, Alkhamesi NA. Endoscopic tattoo: the importance and need for standardised guidelines and protocol. J R Soc Med. Jul 2017;110(7):287–291. doi:10.1177/0141076817712244 · DOI
  18. Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. Jama. Apr 19 2000;283(15):2008–12. doi:10.1001/jama.283.15.2008 · DOI · Paper page
  19. Wan X, Wang W, Liu J, Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol. Dec 19 2014;14:135. doi:10.1186/1471-2288-14-135 · DOI · Paper page
  20. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Bmj. Sep 6 2003;327(7414):557 – 60. doi:10.1136/bmj.327.7414.557 · DOI · Paper page
  21. Sterne JAC, Savović J, Page MJ, et al. RoB 2: a revised tool for assessing risk of bias in randomised trials. Bmj. Aug 28 2019;366:l4898. doi:10.1136/bmj.l4898 · DOI · Paper page
  22. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. Sep 2010;25(9):603–5. doi:10.1007/s10654-010-9491-z · DOI · Paper page
  23. Aldecoa I, Montironi C, Planell N, et al. Endoscopic tattooing of early colon carcinoma enhances detection of lymph nodes most prone to harbor tumor burden. Surg Endosc. Feb 2017;31(2):723–733. doi:10.1007/s00464-016-5026-3 · DOI
  24. Chen YT, Wang JY, Wang JW, Chai CY. Preoperative endoscopic tattooing technique improved lymph node retrieval in rectal cancer patients receiving neoadjuvant concurrent chemoradiotherapy. J Clin Pathol. Nov 2019;73(5):267–272. doi:10.1136/jclinpath-2019-206240 · DOI
  25. Cipe G, Cengiz MB, Idiz UO, et al. The Effects of Preoperative Endoscopic Tattooing on Distal Surgical Margin and Ileostomy Rates in Laparoscopic Rectal Cancer Surgery: A Prospective Randomized Study. Surg Laparosc Endosc Percutan Tech. Aug 2016;26(4):301–3. doi:10.1097/sle.0000000000000298 · DOI
  26. Feo CV, Portinari M, Zuolo M, et al. Preoperative endoscopic tattooing to mark the tumour site does not improve lymph node retrieval in colorectal cancer: a retrospective cohort study. J Negat Results Biomed. May 7 2015;14:9. doi:10.1186/s12952-015-0027-7 · DOI
  27. Imaoka K, Yano T, Yoshimitsu M, et al. Preoperative Endoscopic Tattoo Marking Improves Lymph Node Retrieval in Laparoscopic Rectal Resection: A Retrospective Cohort Study. Ann Coloproctol. Sep 16 2021;doi:10.3393/ac.2021.00458.0065 · DOI
  28. Kang J, Park HS, Kim IK, et al. Effect of preoperative colonoscopic tattooing on lymph node harvest in T1 colorectal cancer. Int J Colorectal Dis. Oct 2015;30(10):1349–55. doi:10.1007/s00384-015-2308-5 · DOI
  29. Okada K, Sadahiro S, Ogimi T, et al. Tattooing improves the detection of small lymph nodes and increases the number of retrieved lymph nodes in patients with rectal cancer who receive preoperative chemoradiotherapy: A randomized controlled clinical trial. Am J Surg. Apr 2018;215(4):563–569. doi:10.1016/j.amjsurg.2017.06.030 · DOI
  30. Hershorn O, Park J, Singh H, Clouston K, Vergis A, Helewa RM. Rates and predictors of repeat preoperative endoscopy for elective colorectal resections: how can we avoid repeated procedures? Surg Endosc. Jun 2022;36(6):4115–4123. doi:10.1007/s00464-021-08733-2 · DOI
  31. Elarini T, Wexner SD, Isenberg GA. The need for standardization of colonoscopic tattooing of colonic lesions. Dis Colon Rectum. Feb 2015;58(2):264–7. doi:10.1097/dcr.0000000000000304 · DOI
  32. Vogel JD, Felder SI, Bhama AR, et al. The American Society of Colon and Rectal Surgeons Clinical Practice Guidelines for the Management of Colon Cancer. Dis Colon Rectum. Feb 1 2022;65(2):148–177. doi:10.1097/dcr.0000000000002323 · DOI
  33. You YN, Hardiman KM, Bafford A, et al. The American Society of Colon and Rectal Surgeons Clinical Practice Guidelines for the Management of Rectal Cancer. Dis Colon Rectum. Sep 2020;63(9):1191–1222. doi:10.1097/dcr.0000000000001762 · DOI
  34. Wlodarczyk J, Kim D, Finney C, Gupta A, Cannom R, Duldulao M. Inking outside the box: systematic review on the utility of tattooing lesions in rectal cancer. Int J Colorectal Dis. Oct 2022;37(10):2101–2112. doi:10.1007/s00384-022-04239-y · DOI

Metadata

Authors
Nawras, M., Chawla, K., DeRiso, A., Dubchuk, C., Beran, A., Aziz, M., & Pannell, S.
Affiliations
  • University of Toledo (US)
  • Indiana University School of Medicine (US)
Corresponding author
Nawras, Mohamad
Venue
International Journal of Colorectal Disease
Published
2023-05-23
Volume
38
Issue
1
Pages
166-166
ISSN
0179-1958 (ISSN-L)
OpenAlex
W4379967500
Cited by
3
References
1
Citations by year
2026: 1 · 2025: 2
FWCI
0.10
Type
journal article
Language
en
Open access
Locations
  • International Journal of Colorectal Disease (publishedVersion)
  • Research Square (acceptedVersion, cc-by)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Oncology › Colorectal Cancer Surgical Treatments
  • Health Sciences › Medicine › Oncology › Colorectal Cancer Screening and Detection
  • Health Sciences › Medicine › Oncology › Gastric Cancer Management and Outcomes
Keywords
endoscopic tattooing, lymph node yield, colorectal cancer, rectal cancer, colon cancer, surgical resection
MeSH terms
Colonic Neoplasms, Humans, Lymph Node Excision, Lymph Nodes, Preoperative Care, Rectal Neoplasms, Retrospective Studies, Tattooing, Colorectal Neoplasms

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review