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The effect of preoperative endoscopic tattooing using India ink on lymph node yield in laparoscopic colectomy for stage I right-sided colon cancer

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Abstract

Purpose

The purpose of this study is to evaluate the effect of preoperative endoscopic tattooing using India ink (ETI) on the number of retrieved lymph nodes (LNs) dissected during laparoscopic surgery for stage I right-sided colon cancer (RCC).

Methods

This single-center, retrospective study included stage I RCC patients who underwent laparoscopic surgery between January 2010 and December 2021. The clinicopathological background and number of LNs retrieved were compared between patients managed with and without ETI. A multiple linear regression analysis was used to examine the effect of independent variables on the LN yield.

Results

A total of 169 patients were enrolled. Of these, 89 patients (52.7%) were classified into the ETI group, and 80 (47.3%) were classified into the no-ETI group. There were no significant differences in age, sex, body mass index, or tumor progression between the two groups. A univariate analysis showed that the number of LNs retrieved was significantly higher in female (26 vs. 24, p = 0.026), with tumor localization in the ascending or transverse colon (20 in the cecum, 26 in the ascending colon, 27 in the transverse colon, p < 0.001), and with preoperative ETI (28 vs. 21, p < 0.001). In a multivariate linear regression analysis, female sex (p = 0.0011), D3 lymphadenectomy (p = 0.046), and preoperative ETI (p = 0.012) were independently associated with the LN yield.

Conclusion

In laparoscopic surgery for stage I RCC, preoperative ETI increased the number of LNs retrieved and allowed for appropriate staging.

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Data availability

The collected data or related documents will not be made available to others.

References

  1. Sung H, Ferlay J, Siegel RL et al (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249. https://doi.org/10.3322/CAAC.21660

    Article  PubMed  Google Scholar 

  2. Schmoll HJ, van Cutsem E, Stein A et al (2012) ESMO Consensus Guidelines for management of patients with colon and rectal cancer. a personalized approach to clinical decision making. Ann Oncol 23:2479–2516. https://doi.org/10.1093/ANNONC/MDS236

    Article  CAS  PubMed  Google Scholar 

  3. Engstrom PF, Arnoletti JP, Benson AB et al (2009) Colon cancer. J Natl Compr Canc Netw 7:778–831. https://doi.org/10.6004/JNCCN.2009.0056

    Article  PubMed  Google Scholar 

  4. Baxter NN, Kennedy EB, Bergsland E et al (2022) Adjuvant therapy for stage II colon cancer: ASCO guideline update. J Clin Oncol 40:892–910. https://doi.org/10.1200/JCO.21.02538

    Article  CAS  PubMed  Google Scholar 

  5. Cai Y, Cheng G, Lu X et al (2020) The re-evaluation of optimal lymph node yield in stage II right-sided colon cancer: is a minimum of 12 lymph nodes adequate? Int J Colorectal Dis 35:623–631. https://doi.org/10.1007/s00384-019-03483-z

    Article  PubMed  Google Scholar 

  6. Märkl B (2015) Stage migration vs. immunology: The lymph node count story in colon cancer. World J Gastroenterol 21:12218–12233. https://doi.org/10.3748/WJG.V21.I43.12218

    Article  PubMed  PubMed Central  Google Scholar 

  7. Törnroos A, Garvin S, Olsson H (2009) The number of identified lymph node metastases increases continuously with increased total lymph node recovery in pT3 colon cancer. Acta Oncol (Madr) 48:1152–1156. https://doi.org/10.3109/02841860902896097

    Article  Google Scholar 

  8. Joosten JJA, Strobbe LJA, Wauters CAP et al (1999) Intraoperative lymphatic mapping and the sentinel node concept in colorectal carcinoma. Br J Surg 86:482–486. https://doi.org/10.1046/J.1365-2168.1999.01051.X

    Article  CAS  PubMed  Google Scholar 

  9. Wakeman C, Yu V, Chandra R et al (2011) Lymph node yield following injection of patent blue V dye into colorectal cancer specimens. Colorectal Dis 13:. https://doi.org/10.1111/J.1463-1318.2011.02673.X

  10. Murawa D, Nowaczyk P, Hünerbein M et al (2011) One hundred consecutive cases of sentinel lymph node mapping in colon cancer-the results of prospective, single–centre feasibility study with implementation of immunohistochemical staining. Int J Colorectal Dis 26:897–902. https://doi.org/10.1007/S00384-011-1182-Z

    Article  PubMed  Google Scholar 

  11. 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 145:826–830. https://doi.org/10.1001/ARCHSURG.2010.180

    Article  PubMed  Google Scholar 

  12. Wlodarczyk J, Kim D, Finney C et al (2022) Inking outside the box: systematic review on the utility of tattooing lesions in rectal cancer. Int J Colorectal Dis 37:2101–2112. https://doi.org/10.1007/S00384-022-04239-Y

    Article  PubMed  Google Scholar 

  13. Imai K, Hotta K, Ito S et al (2017) Use of a novel shorter minimum caliber needle for creating endoscopic tattoos for preoperative localization: a comparative ex vivo study. Endosc Int Open 05:E513–E517. https://doi.org/10.1055/S-0043-106182

    Article  Google Scholar 

  14. Imai K, Hotta K, Ito S et al (2021) Small-dose endoscopic tattooing using a novel needle for localization prior to laparoscopic surgery of colorectal cancer. Dig Dis Sci 66:4448–4456. https://doi.org/10.1007/S10620-020-06757-7

    Article  CAS  PubMed  Google Scholar 

  15. Brierley JD, Gospodarowicz MK, Wittekind C, UICC (2017) TNM classification of malignant tumours, 8th edn. Chichester, West Sussex, UK: Wiley-Blackwell

    Google Scholar 

  16. Hashiguchi Y, Muro K, Saito Y et al (2020) Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol 25:1–42. https://doi.org/10.1007/s10147-019-01485-z

    Article  PubMed  Google Scholar 

  17. Foo CC, Ku C, Wei R et al (2020) How does lymph node yield affect survival outcomes of stage I and II colon cancer? World J Surg Oncol 18. https://doi.org/10.1186/S12957-020-1802-6

  18. Lykke J, Rosenberg J, Jess P, Roikjaer O (2019) Lymph node yield and tumour subsite are associated with survival in stage I-III colon cancer: results from a national cohort study. World J Surg Oncol 17. https://doi.org/10.1186/S12957-019-1604-X

  19. Lykke J, Roikjær O, Jess P (2013) The relation between lymph node status and survival in Stage I-III colon cancer: results from a prospective nationwide cohort study. Colorectal Dis 15:559–565. https://doi.org/10.1111/CODI.12059

    Article  CAS  PubMed  Google Scholar 

  20. Xie D, Song X, Tong L (2021) Stage migration resulting from inadequate number of examined lymph nodes impacts prognosis in stage II colon cancer after radical surgery. Int J Colorectal Dis 36:959–969. https://doi.org/10.1007/S00384-020-03794-6

    Article  PubMed  Google Scholar 

  21. Douaiher J, Hussain T, Langenfeld SJ (2019) Predictors of adequate lymph node harvest during colectomy for colon cancer. Am J Surg 218:113–118. https://doi.org/10.1016/J.AMJSURG.2018.08.020

    Article  PubMed  Google Scholar 

  22. Lykke J, Jess P, Roikjær O (2016) A high lymph node yield in colon cancer is associated with age, tumour stage, tumour sub-site and priority of surgery. Results from a prospective national cohort study. Int J Colorectal Dis 31:1299–1305. https://doi.org/10.1007/S00384-016-2599-1

    Article  PubMed  Google Scholar 

  23. da Costa DW, van Dekken H, Witte BI et al (2015) Lymph node yield in colon cancer: individuals can make the difference. Dig Surg 32:269–274. https://doi.org/10.1159/000381863

    Article  PubMed  Google Scholar 

  24. Kakizoe M, Watanabe J, Suwa Y et al (2021) The histopathological evaluation based on the indocyanine green fluorescence imaging of regional lymph node metastasis of splenic flexural colon cancer by near-infrared observation. Int J Colorectal Dis 36:717–723. https://doi.org/10.1007/S00384-020-03798-2

    Article  PubMed  Google Scholar 

  25. Braat AE, Oosterhuis JWA, Moll FCP, de Vries JE (2004) Successful sentinel node identification in colon carcinoma using Patent Blue V. Eur J Surg Oncol 30:633–637. https://doi.org/10.1016/j.ejso.2004.03.017

    Article  CAS  PubMed  Google Scholar 

  26. Lal N, Chan DKH, Ng ME et al (2022) Primary tumour immune response and lymph node yields in colon cancer. Br J Cancer 126:1178–1185. https://doi.org/10.1038/S41416-022-01700-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rössler O, Betge J, Harbaum L et al (2017) Tumor size, tumor location, and antitumor inflammatory response are associated with lymph node size in colorectal cancer patients. Mod Pathol 30:897–904. https://doi.org/10.1038/MODPATHOL.2016.227

    Article  PubMed  Google Scholar 

  28. Betge J, Harbaum L, Pollheimer MJ et al (2017) Lymph node retrieval in colorectal cancer: determining factors and prognostic significance. Int J Colorectal Dis 32:991–998. https://doi.org/10.1007/S00384-017-2778-8

    Article  PubMed  PubMed Central  Google Scholar 

  29. Ogino S, Nosho K, Irahara N et al (2009) Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype. Clin Cancer Res 15:6412–6420. https://doi.org/10.1158/1078-0432.CCR-09-1438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Arnold A, Kloor M, Jansen L et al (2017) The association between microsatellite instability and lymph node count in colorectal cancer. Virchows Arch 471:57–64. https://doi.org/10.1007/S00428-017-2150-Y

    Article  CAS  PubMed  Google Scholar 

  31. van Oostendorp S, Elfrink A, Borstlap W et al (2017) Intracorporeal versus extracorporeal anastomosis in right hemicolectomy: a systematic review and meta-analysis. Surg Endosc 31:64–77. https://doi.org/10.1007/S00464-016-4982-Y

    Article  PubMed  Google Scholar 

  32. Allaix ME, Degiuli M, Bonino MA et al (2019) Intracorporeal or extracorporeal ileocolic anastomosis after laparoscopic right colectomy: a double-blinded randomized controlled trial. Ann Surg 270:762–767. https://doi.org/10.1097/SLA.0000000000003519

    Article  PubMed  Google Scholar 

  33. Parsons HM, Tuttle TM, Kuntz KM et al (2011) Association between lymph node evaluation for colon cancer and node positivity over the past 20 years. JAMA 306:1089–1097. https://doi.org/10.1001/jama.2011.1285

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to express their heartfelt gratitude to all endoscopists at the Yokohama City University Medical Center who always provided carefully considered, constructive feedback and valuable comments.

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Authors and Affiliations

  1. Department of Surgery, Gastroenterological Center, Yokohama City University Medical Center, 4-57, Urafune-cho, Minami-ku, Yokohama-shi, 232-0024, Japan

    Kenta Iguchi, Jun Watanabe, Yusuke Suwa, Keigo Chida, Yosuke Atsumi, Masakatsu Numata, Tsutomu Sato, Kazuhisa Takeda & Chikara Kunisaki

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  1. Kenta Iguchi
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  2. Jun Watanabe
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  3. Yusuke Suwa
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Contributions

Kenta Iguchi, Jun Watanabe, Yusuke Suwa, Keigo Chida, Yosuke Atsumi, Masakatsu Numata, Tsutomu Sato, Kazuhisa Takeda and Chikara Kunisaki contributed to the conception and design of the study. Kenta Iguchi, Keigo Chida, and Yosuke Atsumi, prepared data collection. Kenta Iguchi wrote the main manuscript text. All authors reviewed the manuscript and accepted the final version.

Corresponding author

Correspondence to Jun Watanabe.

Ethics declarations

Ethical approval

This study was approved by the institutional review board of Yokohama City University Medical Center (approval No. F221100007) and conformed to the provisions of the Declaration of Helsinki.

Consent to participate

Due to the study’s retrospective nature, written informed consent was not obtained. Therefore, we used the opt-out approach to disclose the study information. Participants were provided with information about this project and were able to decline participation voluntarily.

Conflict of interest

JW reports receiving honoraria for lectures from Johnson and Johnson, Medtronic and Eli Lilly and receiving research funding from Medtronic, AMCO and TERUMO outside the submitted work. All remaining authors declare no conflicts of interest in association with the present study.

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Iguchi, K., Watanabe, J., Suwa, Y. et al. The effect of preoperative endoscopic tattooing using India ink on lymph node yield in laparoscopic colectomy for stage I right-sided colon cancer. Int J Colorectal Dis 38, 77 (2023). https://doi.org/10.1007/s00384-023-04381-1

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