Performing sentinel lymph node biopsy without a hand-held gamma probe – overcoming hurdles through team work: An analysis of our learning curve over five years

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The wide spread adoption of this procedure is however, hampered by the availability of the hand-held gamma probe. Aim: To demonstrate the safety and feasibility of sentinel node biopsy using methylene blue and SPECT CT lymphoscintigraphy. Patients and methods: A retrospective review of the case records of all patients of breast cancer, penile cancer and melanomas who underwent surgery at our Institute between December 2019 and November 2024 was analysed. Demographic data, operative data, pathological reports and follow up data were analysed. Results: Out of a total of 628 patients operated for the above cancers, 70 patients underwent a sentinel lymph node biopsy along with surgery for the primary. Localization was possible in all the patients (100%). The time taken to localize the node decreased from 33 minutes to 16 minutes over the course of the learning curve (percentage change of -50%). The median number of nodes isolated increased by 200% and the seroma in the nodal basin decreased by 26%. Recurrences in the nodal basin were commonest in penile cancer (16.6%), while those in the axilla (6.5%) could be salvaged surgically. Conclusion: Sentinel node biopsy can be safely performed even without a hand-held gamma probe, provided strict inclusion criteria, a double dye technique and a dedicated follow up regimen are adhered to. Sentinel node biopsy breast cancer axilla penile cancer melanoma lymphoscintigraphy methylene blue Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Introduction Sentinel lymph nodes as proposed by Cabanas in 1977 represent the first node/ echelon of nodes which drain an organ [ 1 ]. The idea underlying a sentinel lymph node biopsy (SLNB) for melanoma, penile cancer or breast cancer, is the hypothesis that cancers metastasize in a step-wise pattern – going first to the sentinel lymph node draining the organ and then further up the lymphatic chain [ 2 , 3 ]. So, if the sentinel node is uninvolved, the chances of higher-level nodes being involved by cancer are extremely unlikely. This led to the surgeons trying different techniques to identify the sentinel lymph node, in the pursuit of reducing the significant morbidity attendant on an individual undergoing a radical lymphadenectomy. This morbidity being most apparent as upper/ lower limb edema, the technique found rapid uptake in surgery for breast and penile cancers as well as melanoma of the extremities [ 4 ]. Using colored dyes (isosulfan blue, methylene blue) in combination with Technicium 99m (Tc 99m) labelled radio-active isotopes became the standard procedure for identifying the sentinel lymph node. A hand-held gamma probe was the typical portable instrument used to detect the radioactive isotope during surgery to pinpoint the node and send it for histopathologic examination [ 5 , 6 ]. Serving a significant cohort of cancer patients, our tertiary care center in the Public Sector was hampered by the lack of a hand-held gamma probe [ 7 ]. Brainstorming led to the proposal of using the existing SPECT- CT and gamma camera to identify the node and in certain instances, using a blue dye during surgery to pinpoint it. In this paper, we present our data of the previous five years and hope to demonstrate through our learning curve that we were able to overcome logistic obstacles and provide state-of-the art care to our patients. Patients and methods A retrospective review of the case records of all patients of breast cancer, penile cancer and melanoma of the extremities who were clinically and radiologically node negative and underwent a sentinel lymph node biopsy in our center between December 2019 and November 2024, was performed after obtaining due approval from the Institute Ethics Committee. The data abstracted from the case records included the demographic details of the patient, the tumor, node and metastasis (TNM) stage of the cancer, the histopathologic details, the operative details including time taken to localize the node, blood loss, total operative time, number of nodes identified and complications. Follow up was per protocol for each cancer and the incidence of local, nodal and distant failures documented. Methodology of localizing the sentinel lymph node using SPECT-CT: The patients underwent sentinel lymph node localization by lymphoscintigraphy either on the same day or one day prior to the surgery. The radiopharmaceutical/ radiotracer (tracer) used for this purpose was Tc 99m – Sulfur colloid (Tc 99m - SC). The dosage of Tc 99m – SC ranged from 18.5 to 37 Megabequerel (MBq) (0.5 to 1 milliCurie). The site of injection was based on the type of malignancy. It was periareolar in patients with breast malignancy and perilesional in patients with melanoma, penile and vulvar malignancy. The imaging was done using dual head SPECT-CT gamma camera. After the injection of Tc 99m – SC, a static image was acquired of the injection site. The injection site was gently massaged to enhance the flow of tracer through the lymphatics into the nodes. There was no time gap between the injection of the colloid and starting the detection. As the lymph nodes show lesser tracer localization, when compared to injection site, they are less clearly visualized. To overcome this challenge, the site of injection was physically masked using a small piece of lead metal, which was strapped and held in place. The lead piece reduced the intensity of tracer localization, seen on the gamma camera monitor. This helped in better localization of lymph node. The lymph node was localized using a hot marker which was made of very low quantity of tracer (~ 25 micro-Curie) in a needle cap. The lymph node showed increased tracer localization in field of view of gamma camera, that area was localized with help of hot marker and then it was marked on the skin with permanent ink marker pen. Once the lymph node was localized, Single Photon Emission Computer Tomography (SPECT-CT) of that region was performed using the parameters of 64 x 64 matrix, 64 views with 25 seconds per view. The raw data was then reconstructed into trans axial, coronal and sagittal images for interpretation. The lymph node showing tracer uptake was localized and the approximate depth of the node from the skin was noted which was communicated to the surgeon [Fig. 1 ]. Intraoperative localization: For all locations other than the axilla, an incision was placed directly at the point marked on the skin on SPECT CT. For the axilla, we used a second dye in the form of methylene blue to help us visualize the sentinel node. In the operating suite, 6–8 ml of methylene blue (diluted to 5%) was injected in the peri-areolar location in the intra dermal plane. Gentle massaging of the breast was done. After 5–7 minutes, the axillary incision was given along the hairline and deepened to the extent as obtained from the SPECT-CT. A ruler was used to measure the distance from the skin incision and from the mark placed on the surface to triangulate the node in both the ‘X’ and ‘Y’ axes. The visualized lymphatics were slowly dissected till the node was reached. Monopolar diathermy was avoided as much as feasible. The blue nodes and any non-blue nodes in the vicinity were excised and sent for frozen section analysis. Statistics The continuous variables were analysed as the statistical mean or median and the categorical variables as percentages. The change in the variables (operative time, time taken to identify the node etc) were plotted serially on a graph. A paired t-test was used to assess the statistical significance of the changes noted Outcome measures The two main outcome measures which we sought to determine through this study were: 1. The identification rate of the sentinel lymph node using SPECT-CT and methylene blue in the absence of a handheld gamma probe and 2. The regional / nodal recurrence rate after performing a sentinel lymph node biopsy. Results In the period between December 2019 and November 2024, a total of 628 cases of breast cancer, melanoma, penile cancer and vulvar cancer underwent surgery for the primary and the regional lymph nodes in our center. Of these, 70 (11.1%) patients were node negative as ascertained by clinical examination and a focused ultrasonography of the nodal basin. The majority of these patients were those of early breast cancer – 48 (65.7%) [Fig. 2 ]. The age and demographic features are enumerated in Table 1 , with a significant female preponderance (81.5%) even among the patients with melanoma. Most patients were more than 45 years of age (71,4%) and about 61.4% had associated medical co-morbidities. Table 1 DEMOGRAPHIC CHARACTERISTICS OF THE PATIENT COHORT (N = 70) VARIABLE NUMBER PERCENTAGE AGE > 45 YEARS 50 71.4% GENDER: MALE: FEMALE 13: 57 18.5%: 81.5% ASSOCIATED MEDICAL ILLNESS (DIABETES, HYPERTENSION ETC) 43 61.4% FAMILY HISTORY OF CANCER (IN BREAST CANCER PATIENTS) 4 8.6% The operative parameters which were collected included the time taken to identify the sentinel node, the number of nodes harvested and complications specific to the nodal basin. In addition, the surgery performed for the primary was also documented. [ Table 2 and Fig. 3 ]. Table 2 OPERATIVE VARIABLES OF THE PATIENT COHORT (N = 70) VARIABLE FIRST 20 CASES NEXT 20 CASES LAST 30 CASES PERCENTAGE CHANGE OVER TIME P value MEDIAN TIME TAKEN TO IDENTIFY THE SENTINEL NODES 33 MINUTES 24 MINUTES 16 MINUTES -50% 0.05 MEDIAN NUMBER OF NODES HARVESTED 2 3 4 + 200% 0.03 BLEEDING IN THE NODAL BASIN 20ML 20 ML 20 ML 0% NA SEROMA IN THE NODAL BASIN 8 (40%) 6 (30%) 4 (13.3%) -26.6% 0.07 As shown in Table 2 , the median time from skin incision to identification of the sentinel nodes was more than half an hour (median of 33 minutes) in the first twenty cases and over time, it decreased to 16 minutes in the last 30 cases. The median number of nodes harvested also increased from 2 to 4, primarily because of exploring the region surrounding the initially identified node. There was minimal blood loss during this procedure, as is obvious from the numbers depicted. The incidence of post operative seroma in the operated nodal basin showed a decrease of 26.6% over the course of the learning curve. A paired t-test was used to assess the statistical significance of the changes, and revealed a significant ‘p’ value for the decrease in time taken to identify the node (p < 0.05) and in the number of nodes harvested (p < 0.03). Most patients underwent breast conservation surgery (64%) with or without oncoplasty followed by partial amputation of the penis (16%) and wide local excision of melanoma of the lower extremity (11%), with reconstruction. Isolated cases of mastectomy (3%) for ductal carcinoma in situ (DCIS) and emasculation for penile cancers without lymphatic spread (3%) were the unusual outliers in our patient cohort. Identification of the sentinel node (which was the primary outcome measure) was possible in all the cases (100%), though with a longer duration of surgery in the first 20 patients. Recurrence rates in the nodal basin were considered as surrogates for the false negative rate (FNR) of our technique of performing sentinel lymph node biopsy. 3 out of 48 breast cancer patients developed a nodal recurrence in the ipsilateral axilla (6.5%); (all of whom underwent a salvage axillary dissection) whereas 2 patients of penile cancer (16.6%) developed a recurrence in the regional nodal basin. None of the melanoma or vulvar cancer patients failed regionally. This works out to a false negative rate of 7.1% for the entire patient cohort, which is well below the acceptable rate of 11–13%. [ Table 3 ]. Radiotherapy as an adjuvant was given to 45 patients of breast cancer (93.7%) and to both patients of vulvar cancer. None of the penile cancer patients were given adjuvant radiation. The other parameter which we assessed was the incidence of lymphedema on follow up. None of the patients who underwent an inguinal sentinel lymph node biopsy developed edema. However, 2 patients of breast cancer (4.1%) developed Grade I lymphedema two years after completion of treatment, which responded to conservative management. [ Fig. 4 ] Distant and non-regional failures: 4 patients of breast cancer developed distant metastases on follow up (8.3%) of which only 1 was part of the cohort which failed in the axilla. 2 patients of penile cancer (16.6%) developed non regional metastases (para-aortic and supraclavicular nodes) also, and both of them were those who failed in the inguinal region. 2 patients of melanoma developed liver metastases (25%) without any failure in the inguinal region. [ Fig. 5 ] Follow up: The 4 patients of breast cancer who had distant metastases are on systemic therapy and are alive and doing well. The penile cancer patients and the melanoma patients who developed distant metastases succumbed to their cancers in spite of systemic therapy. Of the cohort therefore, 66 patients are alive – 62 of them without local, regional or distant failure (88.5%). Table 3 Recurrences in the operated nodal basin in the patient cohort (N = 70) CANCER SITE (NODAL BASIN) TOTAL NUMBER RECURRENCES IN THE OPERATED NODAL BASIN (SALVAGED) PERCENTAGE BREAST (AXILLA) 48 3 (3) 6.5% PENILE CANCER (INGUINAL) 12 2 (0) 16.6% VULVAR CANCER (INGUINAL) 2 0 0 MELANOMA (INGUINAL) 8 0 0 Discussion Ramon Cabanas, a urologist from Paraguay in 1977 published his data on the first nodes which drain the penis after performing a series of lymphangiograms, localized them around the superficial epigastric vein and gave them the name “sentinel lymph nodes” [ 1 ]. He did not, for the record, use a blue dye or a radio-colloid isotope. Morton and co-workers later started using lymphoscintigraphy and blue dyes to identify the sentinel nodes in melanomas [ 8 , 9 ]. The added advantage of a combination of a blue dye and a hand-held probe to visually and acoustically guide the surgeon to the sentinel lymph node was reported for the first time by Alex, Krag and others in breast cancer [ 10 , 11 ]. There was rapid acceptance of this technique due to the perceived benefits of decreased rates of lymphedema, but with the caveat that it should be performed in high volume centers with sufficient expertise in these cancers (as per the guidelines of management of breast cancer, melanomas and penile cancers) In spite of being a tertiary care center treating high volumes of breast cancer, penile cancer and melanoma, we were hampered by the absence of a hand-held gamma probe and were reluctant to start the sentinel node biopsy program with the blue dye alone, because of the high false negative rates involved in a single localization technique with the study by Gupta et al [ 12 ] showing a 8.6% false negative rate with methylene blue alone compared to 4.3% with a combination of methylene blue and radio colloid. In an effort to offer state-of-the art surgery to our patients, we planned to use the available SPECT CT gamma camera to localize the node and methylene blue intra operatively, especially in the axilla. This data is an analysis of our attempt over the past few years. We adopted stringent inclusion criteria – which was a clinically negative draining basin followed by a focused ultrasonogram of the regional nodal basin to term it as an N0 cancer. The cancers presenting to us were also of a uniformly higher stage, which is common in the Indian setting. This explains the low percentage (11.1%) of patients who were eligible for the sentinel node procedure. The injection sites described in the breast are manifold – periareolar, sub areolar, subdermal, intra dermal, peri-tumoral etc. We followed a periareolar technique of injection, as this has been shown in multiple studies to have a higher localization rate [ 13 , 14 ]. For penile cancers and melanomas, we followed the peritumoral injection technique, as mentioned in literature [ 15 ]. Identification of the sentinel node during lymphoscintigraphy and intra-operatively was 100%. There were no instances where the node was identified by SPECT – CT and not by methylene blue. There were no failures to identify the sentinel nodes – this correlates well with other studies where a detection rate of 98.5% is standard even when a hand held gamma probe is used [ 16 , 17 ]. The time taken to identify the node was about 33 minutes in the initial twenty patients – the maximum time being spent in identifying axillary sentinel nodes when compared to inguinal nodes. This gradually came down to a median time taken of 16 minutes in the last twenty patients. This is also in sync with the average time of 15 to 40 minutes mentioned in various studies [ 18]. There were no significant complications due to the procedure in our study. The two criteria of performing an adequate sentinel node biopsy are a. the number of nodes harvested and b. the false negative rate. The initial cases had a median of two (2) nodes harvested and this improved to four (4) as our experience in doing the procedure increased. At least two nodes need to be harvested at a minimum in these cancers [ 19] for the false negative rate to be low and for us to be sure that we have not missed an involved node in the regional basin. These numbers are the same as reported by other authors using a hand-held gamma probe [ 20 ]. Using recurrences in the nodal basin as a surrogate for the false negative rate (FNR), we arrived at an FNR of 6.5% for breast cancers and this is exceptionally low because the accepted cut off is between 9–11%. A 16.5% recurrence rate in the groin is unacceptable [ 21 ], even though these two patients presented with non-regional metastases simultaneously and the question whether it was a surgical miss or tumor biology is not answered conclusively. Using indocyanine green or a low-cost fluorescein dye in combination with methylene blue would be a viable option where Tc 99m sulfur colloid is unavailable, but it would pre-suppose the availability of a fluorescence detector [ 22 ] Only two patients (4.1%) of axillary sentinel node biopsy developed Grade I lymphedema on follow-up, which would have been due to the use of monopolar diathermy for dissection during the initial few patients, and possible disruption of lymphatics in the axilla. This could be managed with conservative measures and resolved. In spite of extensive evaluation and stringent inclusion criteria, 8.1% of breast cancer and 16.6% of the penile cancers and 25% of the melanoma patients had distant failures, which can be ascribed to tumor biology [ 23 ]. Conclusion Sentinel lymph node biopsy is the standard of care in a node negative axilla for breast cancer, and in a node negative patient with penile cancer and melanoma. Though using a blue dye alone has been recommended by a few authors, combining it with a radio colloid will drastically reduce the false negative rate. Not possessing a hand-held gamma probe should not come in the way of performing this procedure (though with strict quality control measures), as we have demonstrated in this paper. Limitations Dynamic imaging leaves no doubt that the identified node is indeed the sentinel node. The uncertainties in our study are reflected in the false negative rate, which is unacceptably high in penile cancers. Also, the use of indocyanine green may render the use of a gamma probe obsolete in the coming years [ 24 ]. Declarations Consent to participate: An informed, written consent was obtained from each subject for the treatment and for abstracting the blinded data for research and publication purposes, as mandated by the Institutional guidelines Funding declaration: This is an academic study, and has not received funding from any agency, governmental or private. No funding to declare Name of the approval committee: NIMS Institutional Ethics Committee (NIEC); Ref number EC/NIMS/3082/2022 Conflict of interests: The authors declare no conflict of interest Data availability: The blinded data with the confidentiality of the patients protected is stored electronically with the first author, RR References Cabanas RM. An approach for the treatment of penile carcinoma. Cancer. 1977;39:456–66. Hill AD, Tran KN, Akhurst T, et al. Lessons learned from 500 cases of lymphatic mapping for breast cancer. 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The false negative rate of sentinel node biopsy in patients with breast cancer: a meta-analysis. World J Surg. 2012;36(9):2239–51. Sutton R, Kollias J, Prasad V, et al. Same day lymphoscintigraphy and sentinel node biopsy for early breast cancer. ANZ J Surg. 2002;72:542–6. Leijte JA, Hughes B, Graafland NM, et al. Two-center evaluation of dynamic sentinel node biopsy for squamous cell carcinoma of the penis. J Clin Oncol. 2009;27:3325–9. Mark Swerdlow, Kella L, Vangsness, Gavin T, Kress et al. Determining accurate dye combinations for sentinel lymph node detection: a systematic review. Plast Reconstr Surg Glob Open. 2024; 8: 12(2): e 5598. Jakob Kristian Jakobsen. Sentinel node methods in penile cancer – a historical perspective on development of modern concepts. Semin Nucl Med. 2021;52:486–97. Lafreniere AS, Shine JJ, Nicholas CR, et al. The use of indocyanine green and near infrared fluorescence imaging to assist sentinel lymph node biopsy in cutaneous melanoma: a systematic review. Eur J Surg Oncol. 2021;47(5):935–41. Additional Declarations No competing interests reported. Cite Share Download PDF Status: Published Journal Publication published 16 Jul, 2025 Read the published version in World Journal of Surgical Oncology → Version 1 posted Editorial decision: Revision requested 06 May, 2025 Reviews received at journal 05 May, 2025 Reviews received at journal 21 Apr, 2025 Reviewers agreed at journal 14 Apr, 2025 Reviewers agreed at journal 09 Apr, 2025 Reviewers invited by journal 07 Apr, 2025 Submission checks completed at journal 01 Apr, 2025 First submitted to journal 31 Mar, 2025 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. 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Sciences","correspondingAuthor":false,"prefix":"","firstName":"Rachna","middleName":"","lastName":"C","suffix":""},{"id":439271644,"identity":"2de287f7-4ca4-429d-9ac3-31468bcd62db","order_by":5,"name":"Monica Malik","email":"","orcid":"","institution":"Nizam's Institute of Medical Sciences","correspondingAuthor":false,"prefix":"","firstName":"Monica","middleName":"","lastName":"Malik","suffix":""},{"id":439271645,"identity":"d73e60eb-a25a-4221-a424-a231ddddd195","order_by":6,"name":"Rajashekar Shantappa","email":"","orcid":"","institution":"Nizam's Institute of Medical Sciences","correspondingAuthor":false,"prefix":"","firstName":"Rajashekar","middleName":"","lastName":"Shantappa","suffix":""}],"badges":[],"createdAt":"2025-01-29 15:08:19","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-5925159/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-5925159/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1186/s12957-025-03938-4","type":"published","date":"2025-07-16T16:05:30+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":80285527,"identity":"71da8208-f1a8-4a70-9aad-b56fbcc2f336","added_by":"auto","created_at":"2025-04-10 06:42:11","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":65767,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eTHE LYMPHOSCINTIGRAPHY IMAGES TRIANGULATING THE SENTINEL NODE IN X- AND Y -AXES\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"Picture1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-5925159/v1/c941965a5e3c07b663b661b9.jpg"},{"id":80285529,"identity":"f82268ec-915d-4fd4-abe2-aec479c1e28c","added_by":"auto","created_at":"2025-04-10 06:42:11","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":141809,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eDISTRIBUTION OF SENTINEL LYPH NODE BIOPSIES ACROSS VARIOUS CANCERS (IN PERCENTAGE)\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"Picture2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-5925159/v1/101ecacefa45bbdc0ce99814.jpg"},{"id":80285530,"identity":"a80c52ad-d6ba-4901-b1fb-0bfb2e1317b3","added_by":"auto","created_at":"2025-04-10 06:42:11","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":243107,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eSURGERIES PERFORMED FOR THE PRIMARY TUMOR\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"Picture3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-5925159/v1/46f0c0b70c0e82a84b4e24b7.jpg"},{"id":80286838,"identity":"cbd0966b-5db2-4f3a-9799-5622595f19ba","added_by":"auto","created_at":"2025-04-10 06:58:11","extension":"jpg","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":148533,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003ePERCENTAGE OF PATIENTS (SITE-WISE) WHO DEVELOPED LYMPHEDEMA ON FOLLOW UP\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"Picture4.jpg","url":"https://assets-eu.researchsquare.com/files/rs-5925159/v1/9d615a7ce7876ac25bda731c.jpg"},{"id":80285533,"identity":"fc1fefc4-1f52-4766-88c9-f6b27bf65148","added_by":"auto","created_at":"2025-04-10 06:42:12","extension":"jpg","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":146951,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eSURVIVAL AND ONCOLOGIC OUTCOMES OF THE PATIENT COHORT\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"Picture5.jpg","url":"https://assets-eu.researchsquare.com/files/rs-5925159/v1/c959633c3b522db06a68fb3f.jpg"},{"id":87220927,"identity":"ed646ee2-7aca-445b-a51c-9ffe6b90d4fd","added_by":"auto","created_at":"2025-07-21 16:13:11","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1515925,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5925159/v1/e6ee9c36-7400-41af-93db-011d80da9d06.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Performing sentinel lymph node biopsy without a hand-held gamma probe – overcoming hurdles through team work: An analysis of our learning curve over five years","fulltext":[{"header":"Introduction","content":"\u003cp\u003eSentinel lymph nodes as proposed by Cabanas in 1977 represent the first node/ echelon of nodes which drain an organ [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. The idea underlying a sentinel lymph node biopsy (SLNB) for melanoma, penile cancer or breast cancer, is the hypothesis that cancers metastasize in a step-wise pattern \u0026ndash; going first to the sentinel lymph node draining the organ and then further up the lymphatic chain [\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e, \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e]. So, if the sentinel node is uninvolved, the chances of higher-level nodes being involved by cancer are extremely unlikely.\u003c/p\u003e \u003cp\u003eThis led to the surgeons trying different techniques to identify the sentinel lymph node, in the pursuit of reducing the significant morbidity attendant on an individual undergoing a radical lymphadenectomy. This morbidity being most apparent as upper/ lower limb edema, the technique found rapid uptake in surgery for breast and penile cancers as well as melanoma of the extremities [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eUsing colored dyes (isosulfan blue, methylene blue) in combination with Technicium 99m (Tc 99m) labelled radio-active isotopes became the standard procedure for identifying the sentinel lymph node. A hand-held gamma probe was the typical portable instrument used to detect the radioactive isotope during surgery to pinpoint the node and send it for histopathologic examination [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e, \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eServing a significant cohort of cancer patients, our tertiary care center in the Public Sector was hampered by the lack of a hand-held gamma probe [\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e]. Brainstorming led to the proposal of using the existing SPECT- CT and gamma camera to identify the node and in certain instances, using a blue dye during surgery to pinpoint it. In this paper, we present our data of the previous five years and hope to demonstrate through our learning curve that we were able to overcome logistic obstacles and provide state-of-the art care to our patients.\u003c/p\u003e"},{"header":"Patients and methods","content":"\u003cp\u003e A retrospective review of the case records of all patients of breast cancer, penile cancer and melanoma of the extremities who were clinically and radiologically node negative and underwent a sentinel lymph node biopsy in our center between December 2019 and November 2024, was performed after obtaining due approval from the Institute Ethics Committee. The data abstracted from the case records included the demographic details of the patient, the tumor, node and metastasis (TNM) stage of the cancer, the histopathologic details, the operative details including time taken to localize the node, blood loss, total operative time, number of nodes identified and complications. Follow up was per protocol for each cancer and the incidence of local, nodal and distant failures documented.\u003c/p\u003e \u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eMethodology of localizing the sentinel lymph node using SPECT-CT:\u003c/h2\u003e \u003cp\u003eThe patients underwent sentinel lymph node localization by lymphoscintigraphy either on the same day or one day prior to the surgery. The radiopharmaceutical/ radiotracer (tracer) used for this purpose was Tc 99m \u0026ndash; Sulfur colloid (Tc 99m - SC). The dosage of Tc 99m \u0026ndash; SC ranged from 18.5 to 37 Megabequerel (MBq) (0.5 to 1 milliCurie). The site of injection was based on the type of malignancy. It was periareolar in patients with breast malignancy and perilesional in patients with melanoma, penile and vulvar malignancy. The imaging was done using dual head SPECT-CT gamma camera. After the injection of Tc 99m \u0026ndash; SC, a static image was acquired of the injection site. The injection site was gently massaged to enhance the flow of tracer through the lymphatics into the nodes. There was no time gap between the injection of the colloid and starting the detection. As the lymph nodes show lesser tracer localization, when compared to injection site, they are less clearly visualized. To overcome this challenge, the site of injection was physically masked using a small piece of lead metal, which was strapped and held in place. The lead piece reduced the intensity of tracer localization, seen on the gamma camera monitor. This helped in better localization of lymph node. The lymph node was localized using a hot marker which was made of very low quantity of tracer (~\u0026thinsp;25 micro-Curie) in a needle cap. The lymph node showed increased tracer localization in field of view of gamma camera, that area was localized with help of hot marker and then it was marked on the skin with permanent ink marker pen.\u003c/p\u003e \u003cp\u003eOnce the lymph node was localized, Single Photon Emission Computer Tomography (SPECT-CT) of that region was performed using the parameters of 64 x 64 matrix, 64 views with 25 seconds per view. The raw data was then reconstructed into trans axial, coronal and sagittal images for interpretation. The lymph node showing tracer uptake was localized and the approximate depth of the node from the skin was noted which was communicated to the surgeon [Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e].\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eIntraoperative localization:\u003c/h3\u003e\n\u003cp\u003eFor all locations other than the axilla, an incision was placed directly at the point marked on the skin on SPECT CT.\u003c/p\u003e \u003cp\u003eFor the axilla, we used a second dye in the form of methylene blue to help us visualize the sentinel node. In the operating suite, 6\u0026ndash;8 ml of methylene blue (diluted to 5%) was injected in the peri-areolar location in the intra dermal plane. Gentle massaging of the breast was done. After 5\u0026ndash;7 minutes, the axillary incision was given along the hairline and deepened to the extent as obtained from the SPECT-CT. A ruler was used to measure the distance from the skin incision and from the mark placed on the surface to triangulate the node in both the \u0026lsquo;X\u0026rsquo; and \u0026lsquo;Y\u0026rsquo; axes. The visualized lymphatics were slowly dissected till the node was reached. Monopolar diathermy was avoided as much as feasible. The blue nodes and any non-blue nodes in the vicinity were excised and sent for frozen section analysis.\u003c/p\u003e\n\u003ch3\u003eStatistics\u003c/h3\u003e\n\u003cp\u003eThe continuous variables were analysed as the statistical mean or median and the categorical variables as percentages. The change in the variables (operative time, time taken to identify the node etc) were plotted serially on a graph. A paired t-test was used to assess the statistical significance of the changes noted\u003c/p\u003e\n\u003ch3\u003eOutcome measures\u003c/h3\u003e\u003cp\u003eThe two main outcome measures which we sought to determine through this study were: 1. The identification rate of the sentinel lymph node using SPECT-CT and methylene blue in the absence of a handheld gamma probe and 2. The regional / nodal recurrence rate after performing a sentinel lymph node biopsy.\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eIn the period between December 2019 and November 2024, a total of 628 cases of breast cancer, melanoma, penile cancer and vulvar cancer underwent surgery for the primary and the regional lymph nodes in our center. Of these, 70 (11.1%) patients were node negative as ascertained by clinical examination and a focused ultrasonography of the nodal basin. The majority of these patients were those of early breast cancer \u0026ndash; 48 (65.7%) [Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e].\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eThe age and demographic features are enumerated in Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e, with a significant female preponderance (81.5%) even among the patients with melanoma. Most patients were more than 45 years of age (71,4%) and about 61.4% had associated medical co-morbidities.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eDEMOGRAPHIC CHARACTERISTICS OF THE PATIENT COHORT (N\u0026thinsp;=\u0026thinsp;70)\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eVARIABLE\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eNUMBER\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePERCENTAGE\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eAGE\u0026thinsp;\u0026gt;\u0026thinsp;45 YEARS\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e50\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e71.4%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eGENDER: MALE: FEMALE\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e13: 57\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e18.5%: 81.5%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eASSOCIATED MEDICAL ILLNESS (DIABETES, HYPERTENSION ETC)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e43\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e61.4%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eFAMILY HISTORY OF CANCER (IN BREAST CANCER PATIENTS)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.6%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eThe operative parameters which were collected included the time taken to identify the sentinel node, the number of nodes harvested and complications specific to the nodal basin. In addition, the surgery performed for the primary was also documented. \u003cb\u003e[\u003c/b\u003eTable\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e \u003cb\u003eand\u003c/b\u003e Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e\u003cb\u003e].\u003c/b\u003e\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eOPERATIVE VARIABLES OF THE PATIENT COHORT (N\u0026thinsp;=\u0026thinsp;70)\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"6\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eVARIABLE\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eFIRST 20 CASES\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eNEXT 20 CASES\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eLAST 30 CASES\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003ePERCENTAGE CHANGE OVER TIME\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003eP value\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMEDIAN TIME TAKEN TO IDENTIFY THE SENTINEL NODES\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e33 MINUTES\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e24 MINUTES\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e16 MINUTES\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e-50%\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e0.05\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMEDIAN NUMBER OF NODES HARVESTED\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e+\u0026thinsp;200%\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e0.03\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBLEEDING IN THE NODAL BASIN\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e20ML\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e20 ML\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e20 ML\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e0%\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cspan type=\"BoldUnderline\" class=\"BoldUnderline\" name=\"Emphasis\"\u003eNA\u003c/span\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSEROMA IN THE NODAL BASIN\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8 (40%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e6 (30%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e4 (13.3%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e-26.6%\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e0.07\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eAs shown in Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e, the median time from skin incision to identification of the sentinel nodes was more than half an hour (median of 33 minutes) in the first twenty cases and over time, it decreased to 16 minutes in the last 30 cases. The median number of nodes harvested also increased from 2 to 4, primarily because of exploring the region surrounding the initially identified node. There was minimal blood loss during this procedure, as is obvious from the numbers depicted. The incidence of post operative seroma in the operated nodal basin showed a decrease of 26.6% over the course of the learning curve. A paired t-test was used to assess the statistical significance of the changes, and revealed a significant \u0026lsquo;p\u0026rsquo; value for the decrease in time taken to identify the node (p\u0026thinsp;\u0026lt;\u0026thinsp;0.05) and in the number of nodes harvested (p\u0026thinsp;\u0026lt;\u0026thinsp;0.03).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eMost patients underwent breast conservation surgery (64%) with or without oncoplasty followed by partial amputation of the penis (16%) and wide local excision of melanoma of the lower extremity (11%), with reconstruction. Isolated cases of mastectomy (3%) for ductal carcinoma in situ (DCIS) and emasculation for penile cancers without lymphatic spread (3%) were the unusual outliers in our patient cohort.\u003c/p\u003e \u003cp\u003eIdentification of the sentinel node (which was the primary outcome measure) was possible in all the cases (100%), though with a longer duration of surgery in the first 20 patients. Recurrence rates in the nodal basin were considered as surrogates for the false negative rate (FNR) of our technique of performing sentinel lymph node biopsy. 3 out of 48 breast cancer patients developed a nodal recurrence in the ipsilateral axilla (6.5%); (all of whom underwent a salvage axillary dissection) whereas 2 patients of penile cancer (16.6%) developed a recurrence in the regional nodal basin. None of the melanoma or vulvar cancer patients failed regionally. This works out to a false negative rate of 7.1% for the entire patient cohort, which is well below the acceptable rate of 11\u0026ndash;13%. \u003cb\u003e[\u003c/b\u003eTable\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e\u003cb\u003e].\u003c/b\u003e Radiotherapy as an adjuvant was given to 45 patients of breast cancer (93.7%) and to both patients of vulvar cancer. None of the penile cancer patients were given adjuvant radiation.\u003c/p\u003e \u003cp\u003eThe other parameter which we assessed was the incidence of lymphedema on follow up. None of the patients who underwent an inguinal sentinel lymph node biopsy developed edema. However, 2 patients of breast cancer (4.1%) developed Grade I lymphedema two years after completion of treatment, which responded to conservative management. \u003cb\u003e[\u003c/b\u003eFig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003e\u003cb\u003e]\u003c/b\u003e\u003c/p\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eDistant and non-regional failures:\u003c/h2\u003e \u003cp\u003e4 patients of breast cancer developed distant metastases on follow up (8.3%) of which only 1 was part of the cohort which failed in the axilla. 2 patients of penile cancer (16.6%) developed non regional metastases (para-aortic and supraclavicular nodes) also, and both of them were those who failed in the inguinal region. 2 patients of melanoma developed liver metastases (25%) without any failure in the inguinal region. \u003cb\u003e[\u003c/b\u003eFig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003e\u003cb\u003e]\u003c/b\u003e\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eFollow up:\u003c/h3\u003e\n\u003cp\u003eThe 4 patients of breast cancer who had distant metastases are on systemic therapy and are alive and doing well. The penile cancer patients and the melanoma patients who developed distant metastases succumbed to their cancers in spite of systemic therapy. Of the cohort therefore, 66 patients are alive \u0026ndash; 62 of them without local, regional or distant failure (88.5%).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eRecurrences in the operated nodal basin in the patient cohort (N\u0026thinsp;=\u0026thinsp;70)\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCANCER SITE (NODAL BASIN)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eTOTAL NUMBER\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eRECURRENCES IN THE OPERATED NODAL BASIN (SALVAGED)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003ePERCENTAGE\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBREAST (AXILLA)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003e48\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003e3 (3)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003e6.5%\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePENILE CANCER (INGUINAL)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003e12\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2 (0)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003e16.6%\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eVULVAR CANCER (INGUINAL)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eMELANOMA (INGUINAL)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eRamon Cabanas, a urologist from Paraguay in 1977 published his data on the first nodes which drain the penis after performing a series of lymphangiograms, localized them around the superficial epigastric vein and gave them the name \u0026ldquo;sentinel lymph nodes\u0026rdquo; [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. He did not, for the record, use a blue dye or a radio-colloid isotope. Morton and co-workers later started using lymphoscintigraphy and blue dyes to identify the sentinel nodes in melanomas [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e]. The added advantage of a combination of a blue dye and a hand-held probe to visually and acoustically guide the surgeon to the sentinel lymph node was reported for the first time by Alex, Krag and others in breast cancer [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e, \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e]. There was rapid acceptance of this technique due to the perceived benefits of decreased rates of lymphedema, but with the caveat that it should be performed in high volume centers with sufficient expertise in these cancers (as per the guidelines of management of breast cancer, melanomas and penile cancers)\u003c/p\u003e \u003cp\u003eIn spite of being a tertiary care center treating high volumes of breast cancer, penile cancer and melanoma, we were hampered by the absence of a hand-held gamma probe and were reluctant to start the sentinel node biopsy program with the blue dye alone, because of the high false negative rates involved in a single localization technique with the study by Gupta et al [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e] showing a 8.6% false negative rate with methylene blue alone compared to 4.3% with a combination of methylene blue and radio colloid. In an effort to offer state-of-the art surgery to our patients, we planned to use the available SPECT CT gamma camera to localize the node and methylene blue intra operatively, especially in the axilla. This data is an analysis of our attempt over the past few years.\u003c/p\u003e \u003cp\u003e We adopted stringent inclusion criteria \u0026ndash; which was a clinically negative draining basin followed by a focused ultrasonogram of the regional nodal basin to term it as an N0 cancer. The cancers presenting to us were also of a uniformly higher stage, which is common in the Indian setting. This explains the low percentage (11.1%) of patients who were eligible for the sentinel node procedure.\u003c/p\u003e \u003cp\u003eThe injection sites described in the breast are manifold \u0026ndash; periareolar, sub areolar, subdermal, intra dermal, peri-tumoral etc. We followed a periareolar technique of injection, as this has been shown in multiple studies to have a higher localization rate [\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e]. For penile cancers and melanomas, we followed the peritumoral injection technique, as mentioned in literature [\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eIdentification of the sentinel node during lymphoscintigraphy and intra-operatively was 100%. There were no instances where the node was identified by SPECT \u0026ndash; CT and not by methylene blue. There were no failures to identify the sentinel nodes \u0026ndash; this correlates well with other studies where a detection rate of 98.5% is standard even when a hand held gamma probe is used [\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e, \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e]. The time taken to identify the node was about 33 minutes in the initial twenty patients \u0026ndash; the maximum time being spent in identifying axillary sentinel nodes when compared to inguinal nodes. This gradually came down to a median time taken of 16 minutes in the last twenty patients. This is also in sync with the average time of 15 to 40 minutes mentioned in various studies [ 18]. There were no significant complications due to the procedure in our study.\u003c/p\u003e \u003cp\u003eThe two criteria of performing an adequate sentinel node biopsy are \u003cb\u003ea.\u003c/b\u003e the number of nodes harvested and \u003cb\u003eb.\u003c/b\u003e the false negative rate. The initial cases had a median of two (2) nodes harvested and this improved to four (4) as our experience in doing the procedure increased. At least two nodes need to be harvested at a minimum in these cancers [ 19] for the false negative rate to be low and for us to be sure that we have not missed an involved node in the regional basin. These numbers are the same as reported by other authors using a hand-held gamma probe [\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eUsing recurrences in the nodal basin as a surrogate for the false negative rate (FNR), we arrived at an FNR of 6.5% for breast cancers and this is exceptionally low because the accepted cut off is between 9\u0026ndash;11%. A 16.5% recurrence rate in the groin is unacceptable [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e], even though these two patients presented with non-regional metastases simultaneously and the question whether it was a surgical miss or tumor biology is not answered conclusively.\u003c/p\u003e \u003cp\u003eUsing indocyanine green or a low-cost fluorescein dye in combination with methylene blue would be a viable option where Tc 99m sulfur colloid is unavailable, but it would pre-suppose the availability of a fluorescence detector [\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e]\u003c/p\u003e \u003cp\u003eOnly two patients (4.1%) of axillary sentinel node biopsy developed Grade I lymphedema on follow-up, which would have been due to the use of monopolar diathermy for dissection during the initial few patients, and possible disruption of lymphatics in the axilla. This could be managed with conservative measures and resolved.\u003c/p\u003e \u003cp\u003eIn spite of extensive evaluation and stringent inclusion criteria, 8.1% of breast cancer and 16.6% of the penile cancers and 25% of the melanoma patients had distant failures, which can be ascribed to tumor biology [\u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e].\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eSentinel lymph node biopsy is the standard of care in a node negative axilla for breast cancer, and in a node negative patient with penile cancer and melanoma. Though using a blue dye alone has been recommended by a few authors, combining it with a radio colloid will drastically reduce the false negative rate. Not possessing a hand-held gamma probe should not come in the way of performing this procedure (though with strict quality control measures), as we have demonstrated in this paper.\u003c/p\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eLimitations\u003c/h2\u003e \u003cp\u003eDynamic imaging leaves no doubt that the identified node is indeed the sentinel node. The uncertainties in our study are reflected in the false negative rate, which is unacceptably high in penile cancers. Also, the use of indocyanine green may render the use of a gamma probe obsolete in the coming years [\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e].\u003c/p\u003e \u003c/div\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003e\u003cu\u003eConsent to participate:\u0026nbsp;\u003c/u\u003e\u003c/strong\u003eAn informed, written consent was obtained from each subject for the treatment and for abstracting the blinded data for research and publication purposes, as mandated by the Institutional guidelines\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e\u003cu\u003eFunding declaration:\u0026nbsp;\u003c/u\u003e\u003c/strong\u003eThis is an academic study, and has not received funding from any agency, governmental or private. No funding to declare\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e\u003cu\u003eName of the approval committee:\u0026nbsp;\u003c/u\u003e\u003c/strong\u003eNIMS Institutional Ethics Committee (NIEC); Ref number EC/NIMS/3082/2022\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e\u003cu\u003eConflict of interests:\u0026nbsp;\u003c/u\u003e\u003c/strong\u003eThe authors declare no conflict of interest\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e\u003cu\u003eData availability:\u0026nbsp;\u003c/u\u003e\u003c/strong\u003eThe blinded data with the confidentiality of the patients protected is stored electronically with the first author, RR\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eCabanas RM. An approach for the treatment of penile carcinoma. Cancer. 1977;39:456\u0026ndash;66.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHill AD, Tran KN, Akhurst T, et al. Lessons learned from 500 cases of lymphatic mapping for breast cancer. Ann Surg. 1999;229:528\u0026ndash;35.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eUmberto Veronesi G, Paganelli G, Viale, et al. Sentinel lymph node biopsy and axillary dissection in breast cancer: Results in a large series. J Natl Cancer Inst. 1999;91(4):368\u0026ndash;73.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMoody JA, Ali RF, Carbone AC, et al. Complications of sentinel lymph node biopsy for melanoma \u0026ndash; a systematic review of literature. Eur J Surg Oncol. 2017;43(2):270\u0026ndash;7.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKazuyoshi Motumura C, Egawa Y, Komoike, et al. Sentinel node biopsy for breast cancer: technical aspects and controversies. Breast Cancer. 2007;14:25\u0026ndash;30.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eTafra L, Lannin DR, Swanson MS, et al. Multicenter trial of sentinel node biopsy for breast cancer using both technetium sulfur colloid and isosulfan blue dye. Ann Surg. 2001;233:51\u0026ndash;9.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRanganath R, Monalisa Hui S, Uppin, et al. An audit of breast conservation surgery for breast cancer \u0026ndash; a 7-year experience from Southern India. IJSO. 2023;14:492\u0026ndash;6.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBello DM, Faries MB. The landmark series: MSLT 1, MSLT 2 and DeCOG (management of lymph nodes). Ann Surg Oncol. 2020;27(1):15\u0026ndash;21.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMorton DL, Thompson JF, Alistair J, Cochran, et al. Sentinel node biopsy or nodal observation in melanoma. NEJM. 2006;355:1307\u0026ndash;17.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKrag D, Weaver D, Ashikaga T. The sentinel node in breast cancer \u0026ndash; a multicenter validation study. N Eng J Med. 1998;339:941\u0026ndash;6.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAmit Goyal, Robert G, Newcombe, Robert E, Mansel (ALMANAC study group). Role of routine pre operative lymphoscintigraphy in sentinel node biopsy for breast cancer. Eur J Cancer. 2005;41:238\u0026ndash;43.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eVikas Gupta KVVN, Raju TS, Rao, et al. A randomized trial comparing the efficacy of methylene blue dye alone versus combination of methylene blue dye and radioactive sulfur colloid in sentinel lymph node biopsy in early stage breast cancer patients. Indian J Surg Oncol. 2020;11(2):216\u0026ndash;22.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMc Masters KM, Wong SL, Martin RC, et al. Dermal injection of radioactive colloid is superior to peritumoral injection for breast cancer sentinel lymph node biopsy: results of a multi-institutional study. Ann Surg. 2001;233:676\u0026ndash;87.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBirdwell RL, Smith KL, Betts BJ, et al. Breast cancer: variables affecting sentinel lymph node visualization at preoperative lymphoscintigraphy. Radiology. 2001;220:47\u0026ndash;53.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSadeghi R, Gholami H, Zakavi SR, et al. Accuracy of sentinel lymph node biopsy for inguinal lymph node staging of penile squamous cell carcinoma: systematic review and meta-analysis of literature. J Urol. 2012;187:25\u0026ndash;31.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMotomura K, Noguchi A, Hashizume T, et al. Usefulness of a solid state gamma camera for sentinel node identification in patients with breast cancer. J Surg Oncol. 2005;89:12\u0026ndash;7.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSotirios Chondrogiannis A, Feretti E, Facci, et al. Intra-operative hand held gamma camera for sentinel node detection in patients with breast cancer. Clin Nucl Med. 2013;38:132\u0026ndash;6.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKim T, Guiliano AE, Lyman GH, et al. Lymphatic mapping and sentinel lymph node biopsy in early-stage breast cancer: a meta-analysis. Cancer. 2006;106:4\u0026ndash;16.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePesek S, Ashikaga T, Krag LE, et al. The false negative rate of sentinel node biopsy in patients with breast cancer: a meta-analysis. World J Surg. 2012;36(9):2239\u0026ndash;51.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSutton R, Kollias J, Prasad V, et al. Same day lymphoscintigraphy and sentinel node biopsy for early breast cancer. ANZ J Surg. 2002;72:542\u0026ndash;6.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLeijte JA, Hughes B, Graafland NM, et al. Two-center evaluation of dynamic sentinel node biopsy for squamous cell carcinoma of the penis. J Clin Oncol. 2009;27:3325\u0026ndash;9.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMark Swerdlow, Kella L, Vangsness, Gavin T, Kress et al. Determining accurate dye combinations for sentinel lymph node detection: a systematic review. Plast Reconstr Surg Glob Open. 2024; 8: 12(2): e 5598.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJakob Kristian Jakobsen. Sentinel node methods in penile cancer \u0026ndash; a historical perspective on development of modern concepts. Semin Nucl Med. 2021;52:486\u0026ndash;97.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLafreniere AS, Shine JJ, Nicholas CR, et al. The use of indocyanine green and near infrared fluorescence imaging to assist sentinel lymph node biopsy in cutaneous melanoma: a systematic review. Eur J Surg Oncol. 2021;47(5):935\u0026ndash;41.\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"world-journal-of-surgical-oncology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"wjso","sideBox":"Learn more about [World Journal of Surgical Oncology](http://wjso.biomedcentral.com)","snPcode":"12957","submissionUrl":"https://submission.nature.com/new-submission/12957/3","title":"World Journal of Surgical Oncology","twitterHandle":"@OncoBioMed","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"BMC/SO AJ","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Sentinel node biopsy, breast cancer, axilla, penile cancer, melanoma, lymphoscintigraphy, methylene blue","lastPublishedDoi":"10.21203/rs.3.rs-5925159/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-5925159/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cem\u003e\u003cstrong\u003eBackground: \u003c/strong\u003e\u003c/em\u003eSentinel lymph node biopsy is the standard of care in the management of node negative axilla in breast cancer and in node negative melanomas and penile cancers. The wide spread adoption of this procedure is however, hampered by the availability of the hand-held gamma probe.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cem\u003e\u003cstrong\u003eAim: \u003c/strong\u003e\u003c/em\u003eTo demonstrate the safety and feasibility of sentinel node biopsy using methylene blue and SPECT CT lymphoscintigraphy.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cem\u003e\u003cstrong\u003ePatients and methods: \u003c/strong\u003e\u003c/em\u003eA retrospective review of the case records of all patients of breast cancer, penile cancer and melanomas who underwent surgery at our Institute between December 2019 and November 2024 was analysed. Demographic data, operative data, pathological reports and follow up data were analysed.\u003cem\u003e\u0026nbsp;\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003e\u003cem\u003e\u003cstrong\u003eResults: \u003c/strong\u003e\u003c/em\u003eOut of a total of 628 patients operated for the above cancers, 70 patients underwent a sentinel lymph node biopsy along with surgery for the primary. Localization was possible in all the patients (100%). The time taken to localize the node decreased from 33 minutes to 16 minutes over the course of the learning curve (percentage change of -50%). The median number of nodes isolated increased by 200% and the seroma in the nodal basin decreased by 26%. Recurrences in the nodal basin were commonest in penile cancer (16.6%), while those in the axilla (6.5%) could be salvaged surgically.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cem\u003e\u003cstrong\u003eConclusion: \u003c/strong\u003e\u003c/em\u003eSentinel node biopsy can be safely performed even without a hand-held gamma probe, provided strict inclusion criteria, a double dye technique and a dedicated follow up regimen are adhered to.\u003c/p\u003e","manuscriptTitle":"Performing sentinel lymph node biopsy without a hand-held gamma probe – overcoming hurdles through team work: An analysis of our learning curve over five years","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-04-10 06:42:07","doi":"10.21203/rs.3.rs-5925159/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2025-05-06T15:56:12+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-05-05T12:56:18+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2025-04-21T13:46:56+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"74339508033644166143782916490841603927","date":"2025-04-14T15:06:32+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"187765393866542399580645490636266671433","date":"2025-04-09T06:06:49+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2025-04-07T05:50:43+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2025-04-02T00:43:50+00:00","index":"","fulltext":""},{"type":"submitted","content":"World Journal of Surgical Oncology","date":"2025-03-31T13:23:12+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"world-journal-of-surgical-oncology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"wjso","sideBox":"Learn more about [World Journal of Surgical Oncology](http://wjso.biomedcentral.com)","snPcode":"12957","submissionUrl":"https://submission.nature.com/new-submission/12957/3","title":"World Journal of Surgical Oncology","twitterHandle":"@OncoBioMed","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"BMC/SO AJ","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"c203a762-1f80-40f4-928c-bbc789b7b9f9","owner":[],"postedDate":"April 10th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2025-07-21T16:12:29+00:00","versionOfRecord":{"articleIdentity":"rs-5925159","link":"https://doi.org/10.1186/s12957-025-03938-4","journal":{"identity":"world-journal-of-surgical-oncology","isVorOnly":false,"title":"World Journal of Surgical Oncology"},"publishedOn":"2025-07-16 16:05:30","publishedOnDateReadable":"July 16th, 2025"},"versionCreatedAt":"2025-04-10 06:42:07","video":"","vorDoi":"10.1186/s12957-025-03938-4","vorDoiUrl":"https://doi.org/10.1186/s12957-025-03938-4","workflowStages":[]},"version":"v1","identity":"rs-5925159","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5925159","identity":"rs-5925159","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}