Skip to main content

Advertisement

Log in

A Systematic Review and Meta-analysis of Touch Imprint Cytology and Frozen Section Biopsy and Their Comparison for Evaluation of Sentinel Lymph Node in Breast Cancer

  • Scientific Review
  • Published:
World Journal of Surgery Aims and scope Submit manuscript

Abstract

Introduction

Evaluation of axillary lymph nodes after sentinel lymph node biopsy (SLNB) in breast cancer is mostly done by intra-operative frozen section biopsy (FSB) and/ or touch imprint cytology (TIC). In this systematic review and meta-analysis, we have compared the accuracy of the two modalities.

Methods

PubMed, EMBASE, and Cochrane electronic databases were searched for articles comparing TIC with FSB. Articles were assessed for methodological and reporting quality. The main summary measures were pooled sensitivity, pooled specificity, and diagnostic accuracy using bivariate generalized linear mixed models using random effects.

Results

Fourteen studies were included. The pooled sensitivity, specificity, and diagnostic accuracy for FSB were 78%, 100%, and 98.57%. For TIC, the pooled sensitivity, specificity, and diagnostic accuracy were 74%, 98%, and 98.37%. For both methods, visual inspection of summary ROC curves and of forest plots did not show significant heterogeneity.

Conclusion

TIC showed comparable sensitivity, specificity, and accuracy to FSB and hence can be used as its substitute as a rapid and economical test for the detection of axillary lymph node metastasis during SLNB especially in low-resource settings.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Giuliano AE, Edge SB, Hortobagyi GN (2018) Eighth edition of the AJCC cancer staging manual: breast cancer. Ann Surg Oncol 25:1783–1785. https://doi.org/10.1245/s10434-018-6486-6

    Article  Google Scholar 

  2. Sopik V, Narod SA (2018) The relationship between tumour size, nodal status and distant metastases: on the origins of breast cancer. Breast Cancer Res Treat 170:647–656. https://doi.org/10.1007/s10549-018-4796-9

    Article  Google Scholar 

  3. Carter CL, Allen C, Henson DE (1989) Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer 63(1):181–187. https://doi.org/10.1002/1097-0142

    Article  CAS  Google Scholar 

  4. Lyman GH, Somerfield MR, Giuliano AE (2017) Sentinel lymph node biopsy for patients with early-stage breast cancer: 2016 American society of clinical oncology clinical practice guideline update summary. J Oncol Pract 13:196–198. https://doi.org/10.1200/JOP.2016.019992

    Article  Google Scholar 

  5. Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJ, Mansel RE et al (2014) Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981–22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol 15(12):1303–1310. https://doi.org/10.1016/S1470-2045(14)70460-7

    Article  Google Scholar 

  6. Giuliano AE, Ballman KV, McCall L, Beitsch PD, Brennan MB, Kelemen PR, Ollila DW, Hansen NM, Whitworth PW, Blumencranz PW, Leitch AM, Saha S, Hunt KK, Morrow M (2017) Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: the ACOSOG Z0011 (Alliance) randomized clinical trial. JAMA 318(10):918–926. https://doi.org/10.1001/jama.2017.11470

    Article  Google Scholar 

  7. Kamiński JP, Case D, Howard-McNatt M, Geisinger KR, Levine EA (2010) Sentinel lymph node intraoperative imprint cytology in patients with breast cancer-costly or cost effective? Ann Surg Oncol 17(11):2920–2925. https://doi.org/10.1245/s10434-010-1130-0

    Article  Google Scholar 

  8. Whiting PF, Rutjes AW, Westwood ME et al (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536

    Article  Google Scholar 

  9. Moses LE, Shapiro D, Littenberg B (1993) Combining independent studies of a diagnostic test into a summary ROC curve: data-analytic approaches and some additional considerations. Stat Med 12:1293–1316

    Article  CAS  Google Scholar 

  10. Aihara T, Munakata S, Morino H, Takatsuka Y (2004) Comparison of frozen section and touch imprint cytology for evaluation of sentinel lymph node metastasis in breast cancer. Ann Surg Oncol 11(8):747–750

    Article  Google Scholar 

  11. Safai A, Razeghi A, Monabati A, Azarpira N, Talei A (2012) Comparing touch imprint cytology, frozen section analysis, and cytokeratin immunostaining for intraoperative evaluation of axillary sentinel lymph nodes in breast cancer. Indian J Pathol Microbiol 55(2):183–186

    Article  Google Scholar 

  12. Hashmi AA, Naz S, Ahmed O et al (2021) Diagnostic accuracy of intraoperative touch imprint cytology for the diagnosis of axillary sentinel lymph node metastasis of breast cancer: comparison with intraoperative frozen section evaluation. Cureus 13(1):e12960. https://doi.org/10.7759/cureus.12960

    Article  Google Scholar 

  13. Celebioglu F, Sylvan M, Perbeck L, Bergkvist L, Frisell J (2006) Intraoperative sentinel lymph node examination by frozen section, immunohistochemistry and imprint cytology during breast surgery-a prospective study. Eur J Cancer 42(5):617–620

    Article  CAS  Google Scholar 

  14. Lumachi F, Marino F, Zanella S, Chiara GB, Basso SM (2012) Touch imprint cytology and frozen-section analysis for intraoperative evaluation of sentinel nodes in early breast cancer. Anticancer Res 32(8):3523–3526

    Google Scholar 

  15. Francz M, Egervari K, Szollosi Z (2011) Intraoperative evaluation of sentinel lymph nodes in breast cancer: comparison of frozen sections, imprint cytology and immunocytochemistry. Cytopathology 22(1):36–42

    Article  CAS  Google Scholar 

  16. Liang R, Craik J, Juhasz ES, Harman CR (2003) Imprint cytology versus frozen section: intraoperative analysis of sentinel lymph nodes in breast cancer. ANZ J Surg 73:597–599

    Article  Google Scholar 

  17. Sun L, Chen G, Zhou Y et al (2017) Clinical significance of MSKCC nomogram on guiding the application of touch imprint cytology and frozen section in intraoperative assessment of breast sentinel lymph nodes. Oncotarget 8(44):78105–78112. https://doi.org/10.18632/oncotarget.17490

    Article  Google Scholar 

  18. Abe M, Yamada T, Nakano A (2020) Prospective comparison of intraoperative touch imprint cytology and frozen section histology on axillary sentinel lymph nodes in early breast cancer patients. Acta Cytol 64(5):492–497. https://doi.org/10.1159/000508016

    Article  Google Scholar 

  19. Motomura K, Inaji H, Komoike Y, Kasugai T, Nagumo S, Noguchi S, Koyama H (2000) Intraoperative sentinel lymph node examination by imprint cytology and frozen sectioning during breast surgery. Br J Surg 87:597–601

    Article  CAS  Google Scholar 

  20. Petropoulou T, Kapoula A, Mastoraki A et al (2017) Imprint cytology versus frozen section analysis for intraoperative assessment of sentinel lymph node in breast cancer. Breast Cancer (Dove Med Press) 9:325–330. https://doi.org/10.2147/BCTT.S130987

    Article  CAS  Google Scholar 

  21. Van Diest PJ, Torrenga H, Borgstein PJ, Pijpers R, Bleichrodt RP, Rahusen FD, Meijer S (1999) Reliability of intraoperative frozen section and imprint cytological investigation of sentinel lymph nodes in breast cancer. Histopathology 35:14–18

    Article  Google Scholar 

  22. Upender S, Mohan H, Handa U, Attri AK (2009) Intraoperative evaluation of sentinel lymph nodes in breast carcinoma by imprint cytology, frozen section and rapid immunohistochemistry. Diagn Cytopathol 37(12):871–875

    Article  Google Scholar 

  23. Seenu V, Mathur S, Suhani et al (2022) Combined frozen section and imprint smear assessment of sentinel node improves accuracy and reduces false negative rates in breast cancer: a prospective study. Indian J Surg 84:335–339. https://doi.org/10.1007/s12262-021-02877-0

    Article  Google Scholar 

  24. Tew K, Irwig L, Matthews A, Crowe P, Macaskill P (2005) Meta-analysis of sentinel node imprint cytology in breast cancer. Br J Surg 92(9):1068–1080. https://doi.org/10.1002/bjs.5139

    Article  CAS  Google Scholar 

  25. Llatjos M, Castella E, Fraile M, Rull M, Julian FJ, Fuste F, Rovira C, Fernandez-Llamazares J (2002) Intraoperative assessment of sentinel lymph nodes in patients with breast carcinoma: accuracy of rapid imprint cytology compared with definitive histologic workup. Cancer 96:150–156

    Article  Google Scholar 

  26. Chen YZ, Zhang JX, Chen JJ, Liu ZB, Huang XY, Cheng JY, Yang WT, Shao ZM, Shen ZZ, Wu J (2011) Factors associated with the misdiagnosis of sentinel lymph nodes using touch imprint cytology for early stage breast cancer. Oncol Lett 2:277–281

    Article  Google Scholar 

  27. Richards AD, Lakhani SR, James DT, Ung OA (2013) Intraoperative imprint cytology for breast cancer sentinel nodes: is it worth it? ANZ J Surg 83:539–544

    Article  Google Scholar 

  28. Creager AJ, Geisinger KR, Perrier ND, Shen P, Shaw JA, Young PR, Case D, Levine EA (2004) Intraoperative imprint cytologic evaluation of sentinel lymph nodes for lobular carcinoma of the breast. Ann Surg 239:61–66

    Article  Google Scholar 

  29. Sai-Giridhar P, Al-Ramadhani S, George D, Gopinath P, Andrews W, Jader S, Brown S, Findlay A, Arkoumani E, Al-Sam S, McKenzie JG, Bradpiece H, Jenkins S et al (2016) A multicentre validation of Metasin: a molecular assay for the intraoperative assessment of sentinel lymph nodes from breast cancer patients. Histopathology 68:875–887

    Article  Google Scholar 

  30. Bettington M, Lakhani SR, Ung OA (2014) Is the one-step nucleic acid amplification assay better for intra-operative assessment of breast sentinel nodes? ANZ J Surg 84:725–729

    Article  Google Scholar 

  31. Somashekhar SP, Agarwal G, Deo SVS et al (2017) Indian solutions for Indian problems-association of breast surgeons of India (ABSI) practical consensus statement, recommendations, and guidelines for the treatment of breast cancer in India. Indian J Surg 79(4):275–285. https://doi.org/10.1007/s12262-017-1666-3

    Article  CAS  Google Scholar 

  32. Rathod V, Jha CK, Sinha U, Singh PK, Kumar A, Bhadani PP, Kumar M (2021) First comprehensive report of clinicopathological profile of breast cancer from Bihar. India Indian J Surg Oncol 12(3):598–602. https://doi.org/10.1007/s13193-021-01404-7

    Article  Google Scholar 

  33. Anand A, Mishra A, Damde H et al (2022) Molecular profile and clinico-pathological characteristics of breast cancer in central India: first investigative report. Indian J Surg Oncol 13:421–425. https://doi.org/10.1007/s13193-022-01502-0

    Article  Google Scholar 

  34. Khanna R, Bhadani S, Khanna S, Pandey M, Kumar M (2011) Touch imprint cytology evaluation of sentinel lymph node in breast cancer. World J Surg 35(6):1254–1259. https://doi.org/10.1007/s00268-011-1094-7

    Article  Google Scholar 

  35. Adhya AK, Kar M, Mohanty R (2019) Touch imprint cytology: a rapid and accurate method for diagnosis of oral cancer. Acta Cytol 63(5):411–416. https://doi.org/10.1159/000500006

    Article  Google Scholar 

  36. Naveed H, Abid M, Hashmi AA et al (2017) Diagnostic accuracy of touch imprint cytology for head and neck malignancies: a useful intra-operative tool in resource limited countries. BMC Clin Pathol 17:25. https://doi.org/10.1186/s12907-017-0063-y

    Article  Google Scholar 

  37. Aali BS, Malekpour R, Nakheii N, Mehdizadeh A (2005) Utility and diagnostic accuracy of fallopian tube touch imprint cytology. Cytopathology 16(5):252–255. https://doi.org/10.1111/j.1365-2303.2005.00269.x

    Article  CAS  Google Scholar 

  38. Arachchi PS, Weerasekera MM, Seneviratne B et al (2018) Imprint cytology: a useful screening test for diagnosis of Helicobacter pylori in resource poor settings. BMC Res Notes 11:481. https://doi.org/10.1186/s13104-018-3592-2

    Article  CAS  Google Scholar 

  39. Kumar Yadav S, Sharma D, Bala Sharma D, Kintu-Luwaga R, Jha CK, Shekhar S (2022) Barriers and challenges in providing standard breast cancer care in low resource settings. Trop Doct. https://doi.org/10.1177/00494755221092899

    Article  Google Scholar 

  40. Ratanawichitrasin A, Biscotti CV, Levy L, Crowe JP (1999) Touch imprint cytological analysis of sentinel lymph nodes for detecting axillary metastases in patients with breast cancer. Br J Surg 86(10):1346–1348

    Article  CAS  Google Scholar 

  41. Valiveru RC, Agarwal G, Agrawal V, Gambhir S, Mayilvaganan S, Chand G, Mishra A, Agarwal A, Mishra SK (2020) Low-cost fluorescein as an alternative to radio-colloid for sentinel lymph node biopsy-a prospective validation study in early breast cancer. World J Surg 44(10):3417–3422. https://doi.org/10.1007/s00268-020-05631-x

    Article  Google Scholar 

  42. Chavda J, Mishra A, Silodia A, Yadav SK, Sharma DB, Sharma D, Khandare M (2022) Validation sentinel lymph node biopsy study in cN0 axilla using low-cost dual dye technique: potential solution for resource poor settings. Breast Cancer Res Treat 193(1):105–110. https://doi.org/10.1007/s10549-022-06556-w

    Article  CAS  Google Scholar 

  43. Lijmer JG, Mol BW, Heisterkamp S, Bonsel GJ, Prins MH, van der Meulen JH et al (1999) Empirical evidence of design-related bias in studies of diagnostic tests. JAMA 282:1061–1066

    Article  CAS  Google Scholar 

Download references

Funding

No funding was received for this work.

Author information

Authors and Affiliations

Authors

Contributions

BS contributed to literature search, figures, data collection, data analysis, and data interpretation. DS conceived the present idea and contributed to planning, revision, and editing of manuscript. SKY contributed to literature search, figures, study design, data collection, data analysis, data interpretation, and writing. SS and CKJ contributed to data analysis and interpretation. This is to declare that all authors have contributed to the study. No part of the manuscript has been sent for consideration elsewhere or published in any International or National journal. The authors clearly certify that there is no aspect of plagiarism. All the conflicts of interest have been clearly defined and the source of grant disclosed. Due ethical permission/consent has been obtained for carrying out the study. In case of any dispute, the authors will be held fully responsible for the statement disclosed in the cover letter. The authors are also aware of the copyright rules and also declare that they will not reproduce any published text without due permission from the journal.

Corresponding author

Correspondence to Sanjay Kumar Yadav.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 20 KB)

Supplementary file2 (DOCX 19 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bharath, S., Sharma, D., Yadav, S.K. et al. A Systematic Review and Meta-analysis of Touch Imprint Cytology and Frozen Section Biopsy and Their Comparison for Evaluation of Sentinel Lymph Node in Breast Cancer. World J Surg 47, 478–488 (2023). https://doi.org/10.1007/s00268-022-06800-w

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00268-022-06800-w

Navigation