European Radiology

, Volume 22, Issue 3, pp 545–550 | Cite as

Percutaneous removal of sentinel lymph nodes in a swine model using a breast lesion excision system and contrast-enhanced ultrasound

  • Ali R. Sever
  • Philippa Mills
  • Jean-Marc Hyvelin
  • Jennifer Weeks
  • Hatice Gumus
  • David Fish
  • Willem Mali
  • Susan E. Jones
  • Peter A. Jones
  • Haresh Devalia
Breast

Abstract

Objectives

To investigate the feasibility of percutaneous removal of the entire sentinel lymph node (SLN) in an animal model using a breast lesion excision system after identifying these nodes using contrast-enhanced ultrasound (CEUS) and intradermal microbubbles.

Methods

Animal studies approval was obtained. SLNs were identified using CEUS and intradermal injection of microbubbles in two young pigs. Microbubbles were mixed with blue dye and injected around the mammary papillae to access lymphatic drainage to the superficial inguinal lymph nodes. When enhancing nodes were identified, the breast lesion excision system (BLES) was used to remove these nodes percutaneously. Both animals then underwent surgical lymph node dissection. Histopathological examination of all the samples was performed.

Results

Removal of the entire SLN was successful in three groins in the pigs. All three nodes were stained with blue dye. No other stained nodes were observed in the node dissection specimens. The nodal architecture of removed lymph nodes was well preserved on microscopy. There were no signs of excess trauma within the biopsy bed.

Conclusion

The results obtained from the swine model demonstrated that it is feasible to remove the entire SLN percutaneously under the guidance of CEUS and microbubbles.

Key Points

Intradermal injection of microbubbles and CEUS can identify sentinel lymph nodes

Ultrasound could then guide percutaneous removal of intact and complete SLNs

We have shown this was feasible in pigs but not yet in humans

This technique may eventually have the potential to reduce futile SLN biopsies.

Keywords

Breast cancer Experimental animal models Microbubbles Sentinel lymph node biopsy Interventional ultrasonography 

Notes

Acknowledgments

We would like to thank Prof. François Tranquart and Dr. Michel Schneider from BRACCO Suisse SA Imaging for inviting ARS, PM and HD to visit and perform this animal study in Bracco Suisse SA, Geneva Research Centre, and Dr Xavier Fouillet from Bracco Suisse for the histological analysis. BRACCO Imaging, S.p.A, Milan, Italy manufactured the contrast agent SonoVue™ and financially supported the investigation. Dr. Jean-Marc Hyvelin works for BRACCO Suisse SA in the Geneva Research Centre. The biopsy equipment was supplied the Intact® breast lesion excision system (BLES, Intact Medical, Framingham, MA, USA).

References

  1. 1.
    Morton DL, Wen DR, Wong JH et al (1992) Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 127:392–399PubMedCrossRefGoogle Scholar
  2. 2.
    Cox CE, Pendas S, Cox JM et al (1998) Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg 227:645–651, discussion 651–653PubMedCrossRefGoogle Scholar
  3. 3.
    Martin RC 2nd, Edwards MJ, Wong SL et al (2000) Practical guidelines for optimal gamma probe detection of sentinel lymph nodes in breast cancer: results of a multi-institutional study. For the University of Louisville Breast Cancer Study Group. Surgery 128:139–144PubMedCrossRefGoogle Scholar
  4. 4.
    Goldberg BB, Merton DA, Liu JB et al (2004) Sentinel lymph nodes in a swine model with melanoma: contrast-enhanced lymphatic US. Radiology 230:727–734PubMedCrossRefGoogle Scholar
  5. 5.
    Wang Y, Wang W, Li J, Tang J (2009) Gray-scale contrast-enhanced ultrasonography of sentinel lymph nodes in a metastatic breast cancer model. Acad Radiol 16:957–962PubMedCrossRefGoogle Scholar
  6. 6.
    Sever A, Broillet A, Schneider M et al (2010) Dynamic visualization of lymphatic channels and sentinel lymph nodes using intradermal microbubbles and contrast-enhanced ultrasound in a Swine model and patients with breast cancer. J Ultrasound Med 29:1699–1704PubMedGoogle Scholar
  7. 7.
    Sever A, Jones S, Cox K, Weeks J, Mills P, Jones P (2009) Preoperative localization of sentinel lymph nodes using intradermal microbubbles and contrast-enhanced ultrasonography in patients with breast cancer. Br J Surg 96:1295–1299PubMedCrossRefGoogle Scholar
  8. 8.
    Sever AR, Mills P, Jones SE et al (2011) Preoperative sentinel node identification with ultrasound using microbubbles in patients with breast cancer. AJR Am J Roentgenol 196:251–256PubMedCrossRefGoogle Scholar
  9. 9.
    Oruwari JU, Chung MA, Koelliker S, Steinhoff MM, Cady B (2002) Axillary staging using ultrasound-guided fine needle aspiration biopsy in locally advanced breast cancer. Am J Surg 184:307–309PubMedCrossRefGoogle Scholar
  10. 10.
    Abe H, Schmidt RA, Kulkarni K, Sennett CA, Mueller JS, Newstead GM (2009) Axillary lymph nodes suspicious for breast cancer metastasis: sampling with US-guided 14-gauge core-needle biopsy–clinical experience in 100 patients. Radiology 250:41–49PubMedCrossRefGoogle Scholar
  11. 11.
    Mills P, Sever A, Weeks J, Fish D, Jones S, Jones P (2010) Axillary ultrasound assessment in primary breast cancer: an audit of 653 cases. Breast J 16:460–463PubMedCrossRefGoogle Scholar
  12. 12.
    Lee MC, Eatrides J, Chau A et al (2011) Consequences of axillary ultrasound in patients with T2 or greater invasive breast cancers. Ann Surg Oncol 18:72–77PubMedCrossRefGoogle Scholar
  13. 13.
    Alvarez S, Añorbe E, Alcorta P, López F, Alonso I, Cortés J (2006) Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: a systematic review. AJR Am J Roentgenol 186:1342–1348PubMedCrossRefGoogle Scholar
  14. 14.
    Britton PD, Goud A, Godward S et al (2009) Use of ultrasound-guided axillary node core biopsy in staging of early breast cancer. Eur Radiol 19:561–569PubMedCrossRefGoogle Scholar
  15. 15.
    Britton PD, Provenzano E, Barter S et al (2009) Ultrasound guided percutaneous axillary lymph node core biopsy: how often is the sentinel lymph node being biopsied? Breast 18:13–16PubMedCrossRefGoogle Scholar
  16. 16.
    March DE, Coughlin BF, Barham RB et al (2003) Breast masses: removal of all US evidence during biopsy by using a handheld vacuum-assisted device–initial experience. Radiology 227:549–555PubMedCrossRefGoogle Scholar
  17. 17.
    Fine RE, Boyd BA, Whitworth PW, Kim JA, Harness JK, Burak WE (2002) Percutaneous removal of benign breast masses using a vacuum-assisted hand-held device with ultrasound guidance. Am J Surg 184:332–336PubMedCrossRefGoogle Scholar
  18. 18.
    Makita T, Saito Y, Watanabe M (1985) Regional anatomy of swine. The Yamaguchi J Vet Med 12:33–58Google Scholar
  19. 19.
    Lyman GH, Giuliano AE, Somerfield MR et al (2005) American Society of Clinical Oncology. American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol 23:7703–7720PubMedCrossRefGoogle Scholar
  20. 20.
    Kim T, Giuliano AE, Lyman GH (2006) Lymphatic mapping and sentinel lymph node biopsy in early-stage breast carcinoma: a metaanalysis. Cancer 106:4–16PubMedCrossRefGoogle Scholar
  21. 21.
    Suga K, Yuan Y, Okada M et al (2004) Breast sentinel lymph node mapping at CT lymphography with iopamidol: preliminary experience. Radiology 230:543–552PubMedCrossRefGoogle Scholar
  22. 22.
    Tangoku A, Yamamoto S, Suga K et al (2004) Sentinel lymph node biopsy using computed tomography-lymphography in patients with breast cancer. Surgery 135:258–265PubMedCrossRefGoogle Scholar
  23. 23.
    Suga K, Yuan Y, Ogasawara N, Okada M, Matsunaga N (2003) Localization of breast sentinel lymph nodes by MR lymphography with a conventional gadolinium contrast agent. Preliminary observations in dogs and humans. Acta Radiol 44:35–42PubMedCrossRefGoogle Scholar
  24. 24.
    Yamagami T, Yuen S, Sawai K, Nishimura T (2004) MR imaging-guided axillary node biopsy for breast cancer: initial findings. Eur Radiol 14:151–156PubMedCrossRefGoogle Scholar
  25. 25.
    Yang WT, Chang J, Metreweli C (2000) Patients with breast cancer: differences in color Doppler flow and gray-scale US features of benign and malignant axillary lymph nodes. Radiology 215:568–573PubMedGoogle Scholar
  26. 26.
    Nathanson SD, Burke M, Slater R, Kapke A (2007) Preoperative identification of the sentinel lymph node in breast cancer. Ann Surg Oncol 14:3102–3110PubMedCrossRefGoogle Scholar
  27. 27.
    Allen SD, Nerurkar A, Della Rovere GU (2011) The breast lesion excision system (BLES): a novel technique in the diagnostic and therapeutic management of small indeterminate breast lesions? Eur Radiol 21:919–924PubMedCrossRefGoogle Scholar
  28. 28.
    Seror JY, Lesieur B, Scheuer-Niro B, Zerat L, Rouzier R, Uzan S (2011) Predictive factors for complete excision and underestimation of one-pass en bloc excision of non-palpable breast lesions with the Intact® breast lesion excision system. Eur J Radiol. doi:10.1016/j.ejrad.2011.01.049

Copyright information

© European Society of Radiology 2011

Authors and Affiliations

  • Ali R. Sever
    • 1
  • Philippa Mills
    • 1
  • Jean-Marc Hyvelin
    • 2
  • Jennifer Weeks
    • 1
  • Hatice Gumus
    • 3
  • David Fish
    • 4
  • Willem Mali
    • 5
  • Susan E. Jones
    • 6
  • Peter A. Jones
    • 6
  • Haresh Devalia
    • 6
  1. 1.Department of RadiologyMaidstone HospitalMaidstoneUK
  2. 2.Bracco Suisse SAGenevaSwitzerland
  3. 3.Department of Radiology, School of MedicineDicle UniversityDiyarbakirTurkey
  4. 4.Department of PathologyMaidstone HospitalMaidstoneUK
  5. 5.Department of RadiologyUniversity Medical Center UtrechtUtrechtThe Netherlands
  6. 6.Department of SurgeryMaidstone HospitalMaidstoneUK

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