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

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

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

Published version of a preprint

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.

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References 35 · Cited by 3

Research works printed but not linked: 33

  1. Xi Y, Xu P (2021) Global colorectal cancer burden in 2020 and projections to 2040. Transl Oncol 14(10):101174. https://doi.org/10.1016/j.tranon.2021.101174 · DOI
  2. Vogel JD, Eskicioglu C, Weiser MR, Feingold DL, Steele SR (2017) The American Society of Colon and Rectal Surgeons Clinical Practice Guidelines for the Treatment of Colon Cancer. Dis Colon Rectum 60(10):999–1017. https://doi.org/10.1097/dcr.0000000000000926 · DOI
  3. Feingold DL, Addona T, Forde KA et al (2004) Safety and reliability of tattooing colorectal neoplasms prior to laparoscopic resection. J Gastrointest Surg 8(5):543–6. https://doi.org/10.1016/j.gassur.2003.12.016 · DOI
  4. Beretvas RI, Ponsky J (2001) Endoscopic marking: an adjunct to laparoscopic gastrointestinal surgery. Surg Endosc 15(10):1202–3. https://doi.org/10.1007/s004640000304 · DOI
  5. Yeung JM, Maxwell-Armstrong C, Acheson AG (2009) Colonic tattooing in laparoscopic surgery - making the mark? Colorectal Dis 11(5):527–30. https://doi.org/10.1111/j.1463-1318.2008.01706.x · DOI
  6. Onitilo AA, Stankowski RV, Engel JM, Doi SA (2013) Adequate lymph node recovery improves survival in colorectal cancer patients. J Surg Oncol 107(8):828–34. https://doi.org/10.1002/jso.23332 · DOI
  7. Roberto S, Piergiorgio D, Antonio ZM (2020) Lymph node staging for colorectal cancer: Green is the new black. Dig Liver Dis 52(12):1379–1380. https://doi.org/10.1016/j.dld.2020.09.028 · DOI
  8. Le Voyer TE, Sigurdson ER, Hanlon AL et al (2003) Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089. J Clin Oncol 21(15):2912–9. https://doi.org/10.1200/jco.2003.05.062 · DOI
  9. Kelder W, Inberg B, Schaapveld M et al (2009) Impact of the number of histologically examined lymph nodes on prognosis in colon cancer: a population-based study in the Netherlands. Dis Colon Rectum 52(2):260–7. https://doi.org/10.1007/DCR.0b013e3181979164 · DOI
  10. Xiao WW, Zhang LN, You KY et al (2018) 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 14(Supplement):S288-s294. https://doi.org/10.4103/0973-1482.235343 · DOI
  11. Chen SL, Bilchik AJ (2006) More extensive nodal dissection improves survival for stages I to III of colon cancer: a population-based study. Ann Surg 244(4):602–10. https://doi.org/10.1097/01.sla.0000237655.11717.50 · DOI
  12. Dawson K, Wiebusch A, Thirlby RC (2010) Preoperative tattooing and improved lymph node retrieval rates from colectomy specimens in patients with colorectal cancers. Arch Surg 145(9):826–30. https://doi.org/10.1001/archsurg.2010.180 · DOI
  13. Nelson BM (2004) Sentinel lymph node biopsies in cancers of the skin, colon, head and neck, and breast. Proc (Bayl Univ Med Cent) 17(2):99–103. https://doi.org/10.1080/08998280.2004.11927962 · DOI
  14. Bartels SA, van der Zaag ES, Dekker E, Buskens CJ, Bemelman WA (2012) The effect of colonoscopic tattooing on lymph node retrieval and sentinel lymph node mapping. Gastrointest Endosc 76(4):793–800. https://doi.org/10.1016/j.gie.2012.05.005 · DOI
  15. Wlodarczyk J, Dewberry S, Yoon D et al (2023) Assessing the Association Between Endoscopic Tattooing and Lymph Node Yield in Rectal Cancer. J Surg Res 281:37–44. https://doi.org/10.1016/j.jss.2022.08.013 · DOI
  16. Goo JJ, Ryu DG, Kim HW et al (2019) 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 54(5):666–672. https://doi.org/10.1080/00365521.2019.1612940 · DOI
  17. Yang M, Pepe D, Schlachta CM, Alkhamesi NA (2017) Endoscopic tattoo: the importance and need for standardised guidelines and protocol. J R Soc Med 110(7):287–291. https://doi.org/10.1177/0141076817712244 · DOI
  18. Stroup DF, Berlin JA, Morton SC et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283(15):2008–12. https://doi.org/10.1001/jama.283.15.2008 · DOI · Paper page
  19. Wan X, Wang W, Liu J, Tong T (2014) Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol 14:135. https://doi.org/10.1186/1471-2288-14-135 · DOI · Paper page
  20. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–60. https://doi.org/10.1136/bmj.327.7414.557 · DOI · Paper page
  21. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–5. https://doi.org/10.1007/s10654-010-9491-z · DOI · Paper page
  22. Aldecoa I, Montironi C, Planell N et al (2017) Endoscopic tattooing of early colon carcinoma enhances detection of lymph nodes most prone to harbor tumor burden. Surg Endosc 31(2):723–733. https://doi.org/10.1007/s00464-016-5026-3 · DOI
  23. Chen YT, Wang JY, Wang JW, Chai CY (2019) Preoperative endoscopic tattooing technique improved lymph node retrieval in rectal cancer patients receiving neoadjuvant concurrent chemoradiotherapy. J Clin Pathol 73(5):267–272. https://doi.org/10.1136/jclinpath-2019-206240 · DOI
  24. Cipe G, Cengiz MB, Idiz UO et al (2016) 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 26(4):301–3. https://doi.org/10.1097/sle.0000000000000298 · DOI
  25. Feo CV, Portinari M, Zuolo M et al (2015) 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 14:9. https://doi.org/10.1186/s12952-015-0027-7 · DOI
  26. Imaoka K, Yano T, Yoshimitsu M et al (2021) Preoperative Endoscopic Tattoo Marking Improves Lymph Node Retrieval in Laparoscopic Rectal Resection: A Retrospective Cohort Study. Ann Coloproctol. https://doi.org/10.3393/ac.2021.00458.0065 · DOI
  27. Kang J, Park HS, Kim IK et al (2015) Effect of preoperative colonoscopic tattooing on lymph node harvest in T1 colorectal cancer. Int J Colorectal Dis 30(10):1349–55. https://doi.org/10.1007/s00384-015-2308-5 · DOI
  28. Okada K, Sadahiro S, Ogimi T et al (2018) 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 215(4):563–569. https://doi.org/10.1016/j.amjsurg.2017.06.030 · DOI
  29. Hershorn O, Park J, Singh H, Clouston K, Vergis A, Helewa RM (2022) Rates and predictors of repeat preoperative endoscopy for elective colorectal resections: how can we avoid repeated procedures? Surg Endosc 36(6):4115–4123. https://doi.org/10.1007/s00464-021-08733-2 · DOI
  30. Elarini T, Wexner SD, Isenberg GA (2015) The need for standardization of colonoscopic tattooing of colonic lesions. Dis Colon Rectum 58(2):264–7. https://doi.org/10.1097/dcr.0000000000000304 · DOI
  31. Vogel JD, Felder SI, Bhama AR et al (2022) The American Society of Colon and Rectal Surgeons Clinical Practice Guidelines for the Management of Colon Cancer. Dis Colon Rectum 65(2):148–177. https://doi.org/10.1097/dcr.0000000000002323 · DOI
  32. You YN, Hardiman KM, Bafford A et al (2020) The American Society of Colon and Rectal Surgeons Clinical Practice Guidelines for the Management of Rectal Cancer. Dis Colon Rectum 63(9):1191–1222. https://doi.org/10.1097/dcr.0000000000001762 · DOI
  33. Wlodarczyk J, Kim D, Finney C, Gupta A, Cannom R, Duldulao M (2022) Inking outside the box: systematic review on the utility of tattooing lesions in rectal cancer. Int J Colorectal Dis 37(10):2101–2112. https://doi.org/10.1007/s00384-022-04239-y · DOI

Metadata

Authors
Nawras, M., Chawla, K., DeRiso, A., Dubchuk, C., Beran, A., Aziz, M., & Pannell, S. M.
Affiliations
  • University of Toledo (US)
  • Indiana University School of Medicine (US)
Corresponding author
Nawras, Mohamad
Venue
International Journal of Colorectal Disease
Published
2023-06-09
Volume
38
Issue
1
Pages
166-166
ISSN
  • 0179-1958 (ISSN-L)
  • 1432-1262
OpenAlex
W4379967500
Cited by
3
References
35
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

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