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  Table of Contents  
Year : 2019  |  Volume : 56  |  Issue : 2  |  Page : 114-118

Optimization of sentinel lymph node identification techniques in the Indian setting: A randomized clinical trial

1 Department of Surgical Disciplines, All India Institute of Medical Sciences, New Delhi, India
2 Department of Pathology, All India Institute of Medical Sciences, New Delhi, India
3 Department of Nuclear Medicine, All India Institute of Medical Sciences, New Delhi, India

Date of Web Publication2-May-2019

Correspondence Address:
V Seenu
Department of Surgical Disciplines, All India Institute of Medical Sciences, New Delhi
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijc.IJC_163_18

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 » Abstract 

INTRODUCTION: The recommended technique of sentinel lymph node biopsy (SLNB) in breast cancer is a combination of blue dye and radiotracer. In the Indian scenario, SLNB is still not routinely practiced due to lack of nuclear medicine facilities and unavailability of isosulfan blue or patent blue violet (PBV). This study was conducted for optimizing SLN identification techniques by comparing the identification rate using PBV and methylene blue (MB) in combination with radiotracer.
MATERIALS AND METHODS: Single-blinded two-arm parallel design randomized control trial was conducted at an apex teaching and research medical institute in India. Patients with axillary LN–negative breast cancer were included. Blue dye and radio tracer were injected preoperatively, and SLNB was performed using a combination technique. Frozen section was performed. Demographic, clinical, radiological, operative, and histopathological data were recorded. Descriptive statistics were used to represent patient characteristics. Baseline characteristics for entire cohort and between groups were compared using Student's t-test for quantitative variables and Chi-square test for qualitative variables.
RESULTS: A total of 119 patients were randomized for mapping with MB and 118 patients with PBV between 2011 and 2015. SLN was identified in 116 patients with MB and 115 with PBV. SLN identification proportions were 97.4% (MB) and 96.6% (PBV). In patients undergoing axillary lymph node dissection, concordance with SLNB was 98.5% and 96.61% in MB and PBV, respectively. False-negative proportion for MB was 2.56% and 7.69% for PBV, respectively. The cost of MB is about INR 15 per ~10-mL vial. The cost of PBV is approximately ~$91 per ampoule (equivalent to approximately INR 8190).
CONCLUSION: SLNB using MB can be recommended as the technique of choice in low-resource settings.

Keywords: Axillary lymph node, blue dye, breast cancer, methylene blue, sentinel lymph node biopsy

How to cite this article:
Seenu V, Suhani S, Srivastava A, Parshad R, Mathur S, Kumar R. Optimization of sentinel lymph node identification techniques in the Indian setting: A randomized clinical trial. Indian J Cancer 2019;56:114-8

How to cite this URL:
Seenu V, Suhani S, Srivastava A, Parshad R, Mathur S, Kumar R. Optimization of sentinel lymph node identification techniques in the Indian setting: A randomized clinical trial. Indian J Cancer [serial online] 2019 [cited 2022 Nov 26];56:114-8. Available from:

 » Introduction Top

Axillary lymph node (LN) involvement remains the most important prognostic variable in nonmetastatic breast cancer.[1] The currently recommended technique of sentinel lymph node biopsy (SLNB) in breast cancer is a combination of blue dye [commonly used isosulfan blue or patent blue violet (PBV)] and radiotracer-guided technique (Tc99m-labeled sulfur colloid).[2] Using this technique, SLNB has been shown to be successful in 92%–94% of cases with accuracy ranging from 98% to 100%.[3],[4]

The currently recommended technique of SLNB in breast cancer is a combination of blue dye (commonly used isosulfan blue or PBV) and radiotracer-guided technique (Tc99m-labeled sulfur colloid). Neither of the blue dyes are currently marketed in India, are expensive to import, and not easily available. Nuclear medicine facilities are not available at most centers, and the hand held gamma probe that is used for intraoperative SLNB is expensive. Thus, there was a long felt need to investigate further to identify a cost-effective and accurate method of SLNB in the Indian setting. Although another blue dye, methylene blue (MB), has been used previously by surgeons with similar identification rates,[5],[6],[7] there are no randomized trials comparing the efficacy of MB vis-à-vis isosulfan blue or PBV for SLNB. This randomized controlled trial was hence conducted with the aim of optimizing SLNB identification techniques by comparing the sentinel lymph node (SLN) identification rate using PBV and MB in combination with radiotracer in clinically negative axillary LN breast cancer.

 » Materials and Methods Top

A single-blinded two-arm parallel design randomized control trial was conducted at an apex teaching and research medical institute in India. All patients with axillary LN–negative (N0) breast cancer were included in the study. Patients with clinically palpable nodes, fine needle aspiration cytology (FNAC) or core needle biopsy–proven axillary LN metastasis, prior history of breast or upper limb surgery, breast or axillary radiotherapy, pregnant or lactating women, and metastatic disease were excluded from the study.

A sample size of 107 patients was calculated using a two-group continuity-corrected χ2 test, assuming that MB identified SLN in 75% of cases and PBV in 85% of cases, with alpha error of 5% and 80% power.

All patients underwent bilateral mammography with ultrasound of the axilla. Patients with suspicious nodes on imaging underwent FNAC. All patients underwent SLNB using a combination technique. Radionuclide tracer was injected in the peritumoral location in the nuclear medicine suite. Patients were then randomized to methylene group (Group I) or PBV group (Group II) using computer-generated random numbers. SLNB using blue dye was done under general anesthesia at the time of primary surgery. About 3–5 mL of blue dye (MB or PBV) was injected intraparenchymal around the tumor using a sterile disposable syringe with 24-G needle at 12, 3, 6, and 9 O'clock positions (1 mL at each location). Then the breast was massaged for 5 min toward axilla to facilitate the uptake of dye into lymphatic and its passage toward axilla. SLNB was done giving a skin crease incision below the hair bearing area in the axilla in cases where breast conservation surgery was planned or via the lateral end of a suitably placed mastectomy incision. SLNB was performed prior to the primary tumor surgery. Hand held gamma probe was used to identify the hot nodes, whereas blue nodes were identified by visual inspection. Any LN that was blue/hot/hot and blue or to which a blue stained lymphatic lead/ended was considered as SLN. Sentinel nodes were removed and subjected to frozen section. Patients who had no metastasis in SLNB did not undergo axillary lymph node dissection (ALND). In other patients, following SLNB, conventional levels I, II, and III ALND was performed.

The demographic, clinical, radiological, operative, and histopathological data of the patients were entered in a predesigned Performa. Descriptive statistics such as mean, median, and range were used to represent patient characteristics. Baseline characteristics for the entire cohort and between the two groups were compared using Student's t-test for quantitative variables and Chi-square test for qualitative variables. The number of patients in whom SLN was identified, the number of nodes identified in each patient, the proportion of positive nodes among the nodes identified, the concordance, and false negativity of the SLN technique by the two dyes were calculated as proportions (%) along with their 95% confidence intervals (CIs).

 » Results Top

A total of 237 patients were mapped for SLN evaluation between 2011 and 2015 to study the objective of comparison of success rates of MB and PBV in SLN mapping. A total of 119 patients were randomized for mapping with MB and 118 patients randomized for mapping with PBV. The CONSORT diagram is shown in [Figure 1].
Figure 1: Consort flow diagram

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The baseline characteristics were distributed equally in the two groups (P > 0.05 for all variables) and are shown in [Table 1].
Table 1: Baseline characteristics of patients in the two groups

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SLN was successfully identified by mapping in 116 of 119 patients in the MB group and 115 of 118 of patients in the PBV group. Thus, the SLN identification proportions are the 97.4% (95% CI: 92.8%–99.4%) and 96.6% (95% CI: 97.4%–99.4%) for MB and PBV, respectively (P > 0.05). [Table 2] summarizes the results of SLN mapping in both the groups.
Table 2: Results of sentinel node mapping

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Sixty-seven patients in MB group and 59 patients in PBV group underwent ALND. Some patients with negative SLNB underwent ALND as part of another ongoing study. The results of SLN and non-SLNs are given in [Table 3].
Table 3: Comparison of SLN mapping results in patients who underwent ALND

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Among patients who underwent ALND, the concordance in MB group and PBV group between SLNB and ALND was 98.5% (95% CI: 91.96%–99.96%; 66 of 67 patients) and 96.61% (95% CI: 88.28%–99.59%; 57 of 59 patients), respectively. The false-negative proportion for MB was 1.49% (1 of 39 patients) and 3.39 (95% CI: 0.94%–25.13%; 2 of 26 patients) for PBV, respectively.

No serious complications occurred in any group. Skin necrosis was present in one patient in the MB group, while blue hives developed in two patients (one at local site and one at distant site) in PB group. The cost of MB is about INR 15 per ~10-mL the vial. The cost of PBV is approximately ~$91 per ampoule (equivalent to INR 8190 approximately).

 » Discussion Top

Although ALND is a safe procedure, long-term squeal are common, including upper arm numbness/tingling (7%–75%), pain (16%–56%), impaired shoulder mobility (4%–45%), arm weakness (19%–35%), lymphangitis (8%), potentially disabling lymphedema (6%–30%), and risk of developing lymphangiosarcoma.[8],[9],[10] The development and acceptance of the SLNB have significantly altered the management of node-negative breast cancer by providing highly accurate and less morbid axillary staging procedure. SLNB alone is associated with less than 1% isolated axillary recurrence in patients with node-negative disease and provides excellent regional nodal control.[11]

The currently recommended technique for SLNB is a combination technique wherein a blue dye and radiotracer are used for detection of SLN.[2] Using the combination technique in our study, the overall SLN identification rate was 97.4% (95% CI: 92.8%–99.4%). Similar results have been reported in various validation studies with SLN identification rates ranging between 92% and 94%.[11],[12] The concordances and false-negative rates reported for SLN vary between 95% and 100% and 5% and 10%, respectively.[11],[13] In our study, in patients in whom ALND was also performed after SLNB, the concordance between SLN status and ALN status was 97.62% and the false negative rate was 4.6%. Thus, the results of this study also show that SLNB accurately predicts axillary nodal status in breast cancer. Also in this subset of patients, the concordances and false-negative rates for MB and PBV were 98.5% and 96.6% and 2.56% and 7.69%, respectively. Though the false-negative proportions in PBV group were slightly higher (7.69%), this difference did not attain statistical significance.

Various dyes studied for SLNB include isosulfan blue, patent blue, MB, and fluorescein dyes.[7] Isosulfan blue and PB have been most widely used because these two were considered to have an apt particle size to be retained in the lymphatics, while MB was thought to have a larger size so as to enter the blood stream preferentially. However, resurgence of interest in MB came after the western world saw an acute shortage of isosulfan blue in the early part of 21st century. Simmons et al. described one for the first reports of successfully using MBD for SLN mapping.[14] Since then, the dye has been studied for the purpose in various prospective studies.[14],[15]

Our results show an overall SLN identification rate of 97.4% with MB as blue dye in combination with radiotracer and 96.6% with PBV combined with radiotracer. These results are similar to those of other investigators using isosulfan/PBV in combination with radiotracer,[3],[4] as well as MB alone or in combination with radiotracer.[6],[7],[14],[15]

The technical success rates of sentinel LN identification using MBD alone vary from 90% to 97%, with the detection rates increasing in recent years, likely due to better training of the surgeons in SLNB.[16],[17],[18] Even in our experience, when MB was used alone for SLN identification in 37 patients outside this study, it showed high success rate (94.5%). This is particularly important as MB can also be even offered as a single agent particularly in resource-limited settings.

There were three failures in each group and all had palpable LNs but not hot/blue or hot and blue nodes in axilla. However, currently many surgeons consider palpable node in axilla also as SLN.[19] As axillary lymphadenopathy also occurs because of many other nonspecific causes, we did not consider palpable lymphadenopathy as SLN to avoid the bias of identification using the blue dye. These cases are summarized in [Table 4].
Table 4: Details of six cases of failure of SLN identification

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In the MB group, 315 nodes were detected in 116 patients (2.73 nodes per case), and in the patent blue group, 302 nodes were detected in 115 patients (2.55 nodes per case). The total number of blue and the total number of hot and blue LNs were similar in both groups (P > 0.05). The mean number of positive nodes in both groups was also similar (P > 0.05). Fifty-five of the 220 blue/hot and blue nodes in MB showed metastasis (25%), whereas 32 of 224 (14.28%) were positive in the PBV group. However, this difference was not statistically significant (P > 0.05). Blessing et al. reported an average of 1.76 nodes per patient among 86 patients who underwent SLNB using Lymphazurin and 1.94 nodes per case in 111 patients who underwent SLNB using MB.[15]

SLN evaluation showed metastasis in 38 of 116 (32.76%) patients in MB group and 24 of 115 (20.87%) patients in PBV group. MB detected 11.89% (95% CI: -03 to 21.8) more patients with positive LNs (38/116; 32.76%) as compared to patent blue (24/115; 20.87%). However, this difference did not reach statistical difference (P > 0.058). Blessing et al. reported positive SLN in 33.9% of patients in using MB when compared with 29.9% using Lymphazurin.[19] Even this difference was not statistically different. These results are similar to those reported in the NSABP-32 trial where SLN was negative in 71.1% of patients.[20]

The incidence of complications was very low following the use of MB (0.84%) or PBV (1.6%). One patient who underwent SLNB with MB had developed skin necrosis at the site of injection. Two patients in the patent blue group developed blue hives – one at the site of injection, which regressed in 72 h, and the other person at the site of injection and at other sites, which also regressed spontaneously in 1 week. In a review, Thevarajah et al. found 1% incidence of complications using isosulfan blue (including allergic life-threatening reactions needing aggressive resuscitation).[21] Life-threatening reactions with MBD have been noted in only one case despite extensive literature search.[22] While isosulphan blue is known to interfere with pulse oxymetry, such changes in recordings for oxygen saturation are reported to be much less with MBD.[23] The most common reported complications following use of MB are formation of mass at injection site secondary to fat necrosis and necrosis of skin if the dye is injected superficially into the skin.[21],[24],[25],[26],[27] The occurance of necrosis at injection site can be avoided by excising the tissue into which MB has been injected by including it in the wide local excision of the primary breast tumor. Also, increasing use of diluted MBD has decreased the incidence of such events.

The cost of performing SLNB was significantly lower when MB was used, with the difference being little more than 8000 INR.

 » Conclusion Top

SLNB using MB is a highly sensitive, cost-effective technique, and can be recommended as the technique of choice (in place of PBV) for the detection of SLN for breast cancer in low-resource settings. Every surgeon opting for this technique should validate their own results to ensure that optimum identification results are being achieved.

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Conflicts of interest

There are no conflicts of interest.

 » References Top

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Consensus statement on guidelines for performing sentinel lymph node dissection in breast cancer. 2008 Feb 28. Available from: [Last accessed on 2017 Dec 24].  Back to cited text no. 2
DeRossis AM, Fey J, Yeung H, Yeh SD, Heerdt AS, Petrek J, et al. A trend analysis of the relative value of blue dye and isotope localization in 2000 consecutive cases of sentinel node biopsy for breast cancer. J Am Coll Surg 2001;193:473-8.  Back to cited text no. 3
Krag D, Weaver D, Ashikaga T, Moffat F, Klimberg VS, Shriver C, et al. The sentinel node in breast cancer – A multicenter validation study. N Engl J Med 1998;339:941-6.  Back to cited text no. 4
Thomas S, Prakash A, Goyal A, Popli MB, Agarwal S, Choudhury M. Evaluation of sentinel node biopsy in locally advanced breast cancer patients who become clinically negative after neo adjuvant chemotherapy: A preliminary study. Int J Breast Cancer 2011;2011:870263.  Back to cited text no. 5
Chintamani, Tandon M, Mishra A, Agarwal U, Saxena S. Sentinel node biopsy using dye alone method is reliable and accurate even neo adjuvant chemotherapy in locally advanced breast cancer. World J Surg Oncol 2011;9:19.  Back to cited text no. 6
Somashekhar SP, Zaveri Shabber S, Udupa Venkatesh K, Venkatachala K, Parameshwaran, Vasan Thirumalai MM. Sentinel lymph node biopsy in early breast cancer using methylene blue dye and radioactive sulphur colloid – A single institution Indian experience. Indian J Surg 2008;70:111-9.  Back to cited text no. 7
Lin PP, Allison DC, Wainstock J, Miller KD, Dooley WC, Friedman N, et al. Impact of axillary lymph node dissection on the therapy of breast cancer patients. J Clin Oncol 1993;11:1536-44.  Back to cited text no. 8
Fisher B, Jeong JH, Anderson S, Bryant J, Fisher ER, Wolmark N. Twenty five year follow-up of a randomized trial comparing radical mastectomy, total mastectomy followed by irradiation. N Engl J Med 2002;347:567-75.  Back to cited text no. 9
Keramopoulos A, Tsionou C, Minaretzious D, Michalas S, Aravantinos D. Arm morbidity following treatment of breast cancer with total axillary dissection: A multivariated approach. Oncology 1993;50:445-9.  Back to cited text no. 10
Cox CE, Pendas S, Cox JM, Joseph E, Shons AR, Yeatman T, et al. Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg 1998;227:645-53.  Back to cited text no. 11
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Simmons R, Thevarajah S, Brennan MB, Christos P, Osborne M. Methylene blue dye as an alternative to isosulfane blue dye for sentinel lymph node localization. Ann Surg Oncol 2003;10:242-7.  Back to cited text no. 14
Blessing WD, Stolier AJ, Teng SC, Bolton JS, Fuhrman GM. A comparison of methylene blue and lymphazurin in breast cancer sentinel node mapping. Am J Surg 2002;184:341-5.  Back to cited text no. 15
Golshan M, Nakhlis F. Can methylene blue only be used in sentinel lymph node biopsy for breast cancer? Breast J 2006;12:428-30.  Back to cited text no. 16
Nour A. Efficacy of methylene blue dye in localization of sentinel lymph node in breast cancer patients. Breast J 2004;10:388-91.  Back to cited text no. 17
Varghese P, Mostafa A, Abdel-Rahman AT, Akberali S, Gattuso J, Canizales A, et al. Methylene blue dye versus combined dye-radioactive tracer technique for sentinel lymph node localisation in early breast cancer. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol 2007;33:147-52.  Back to cited text no. 18
Mansel RE, Fallowfield L, Kissin M, Goyal A, Newcombe RG, Dixon JM, et al. Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: The ALMANAC Trial. J Natl Cancer Inst 2006;98:599-609.  Back to cited text no. 19
Krag DN, Anderson S, Julian T, Brown AM, Harlow SP, Costantino JP, et al. Sentinel lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: Overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol 2010;11:927-33.  Back to cited text no. 20
Thevarajah S, Huston TL, Simmons RM. A comparison of the adverse reactions associated with isosulfan blue versus methylene blue dye in sentinel lymph node biopsy for breast cancer. Am J Surg 2003;189:236-9.  Back to cited text no. 21
Dewachter P, Mouton-Faivre C, Tréchot P, Lleu JC, Mertes PM. Severe anaphylactic shock with methylene blue instillation. Anesth Analg 2005;101:149-50.  Back to cited text no. 22
Piñero A, Illana J, Garcia-Palenciano C, Cañizarese F, Canteras M, Cañadillas V, et al. Effect on oximetry of dyes used for sentinel lymph node biopsy – Are there differences? Arch Surg 2004;139:1204-7.  Back to cited text no. 23
Shirah GR, Bouton ME, Komenaka IK. Occurrence of prolonged injection site mass with methylene blue but not isosulfan blue after the sentinel node procedure. Arch Surg Chic Ill 1960 2011;146:137-41.  Back to cited text no. 24
Kang SS, Han BK, Ko EY, Shin JH, Cho EY, Lee JE, et al. Methylene blue dye-related changes in the breast after sentinel lymph node localization. J Ultrasound Med 2011;30:1711-21.  Back to cited text no. 25
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Reyes F. Complications of methylene blue dye in breast surgery: Case reports and review of the literature. J Cancer 2011;20:202-6.  Back to cited text no. 27


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  [Table 1], [Table 2], [Table 3], [Table 4]

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