Radiography
Volume 18, Issue 1 , Pages 9-14, February 2012

Correlation of number and identification of sentinel nodes during radiographer led lymphoscintigraphy prior to sentinel lymph node biopsy in breast cancer patients

  • Gail Camilleri

      Affiliations

    • Medical Imaging Department, Mater Dei Hospital, Malta
    • Tel.: +356 79921833.
    • ,
  • Karen Borg Grima

      Affiliations

    • Department of Radiography, Faculty of Health Sciences, University of Malta, Malta
    • Tel.: +356 23401812.
    • ,
  • Francis Zarb

      Affiliations

    • Department of Radiography, Faculty of Health Sciences, University of Malta, Malta
    • Corresponding Author InformationCorresponding author. Tel.: +356 23401833; fax: +356 21244975.

Received 28 September 2011; received in revised form 8 November 2011; accepted 11 November 2011. published online 05 December 2011.

Article Outline

Abstract 

Purpose

The sentinel lymph node biopsy (SLNB) concept using the cutaneous (subdermal) peri-areolar approach is rapidly emerging as the technique for axillary staging in breast cancer. The procedure indicates whether axillary lymph node dissection (ALND) is necessary, therefore drastically minimising the invasiveness of surgical treatment. The SLNB concept is based on evidence suggesting that malignant disease primarily affects the sentinel node (SN) before being disseminated into the axillary lymph nodes (ALNs).

Objective

This study was to define the role of lymphoscintigraphy in the visualisation of SNs during SLNB and to establish the correlation between the number of SNs identified on lymphoscintigraphy to the number of surgically identified SNs.

Method

The study was a non-experimental, correlation study utilising quantitative data. Lymphoscintigraphy reports and histology results of 55 female breast cancer patients who underwent SLNB with partial or total back-up ALND, were retrospectively evaluated.

Results

A maximum of 2 and a minimum of 0 sentinel nodes were visualised on lymphoscintigraphy in 52 out of 55 patients. Successful lymphoscintigraphy was highly predictive (p≤0.001) of a successful SLNB as all 52 patients (94.5%) proceeded to have successful SN/s identification. There was a significant association (p≤0.05) between the number of SN/s visualised on lymphoscintigraphy and the number of SN/s identified during SLNB. Lymphoscintigraphy accurately predicted the number of surgically identified SNs in 50.91% of cases (28/55).

Conclusion

Considering that successful imaging effectively assures SN identification, the routine use of lymphoscintigraphy using the subdermal peri-areolar approach is fundamental in the reliable performance of SLNB.

Keywords: Breast cancer, Lymphoscintigraphy, Sentinel lymph node biopsy, Axillary lymph node dissection

 

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Introduction 

Breast cancer is the most common malignant tumour in adult females in industrialised countries.1, 2 With mortality rates in Malta (28.1%) higher than the EU average (23.9%),3 breast cancer presents an enormous public health issue locally.4 Until May 2009, the management of breast cancer patients in Malta involved axillary lymph node dissection (ALND) whereby all the axillary nodes are dissected irrespective of their metastatic involvement. This radical type of approach is an overtreatment in 80% of patients5 as women are unnecessarily subjected to the morbidity of ALND which includes: lymphoedema, neuropathy, paresthaesia and decreased mobility.6, 7

The prognosis of breast cancer prevalence is improved by the innovative approach of the sentinel lymph node biopsy (SLNB) for axillary staging. The SLNB is a minimally invasive surgical technique that provides an accurate alternative to the standard ALND by sparing the patients the removal of the axillary lymph nodes (ALNs) in the absence of axillary metastases, thus improving their quality of life.8, 9, 10 The SLNB is based on the concept of the sentinel node (SN), which postulates that lymph node metastases follow a predictable course.10, 11 The SN is the first encountered lymph node in the axillary basin that receives the lymphatic drainage of the primary tumour. Occasionally, two or more lymphatic channels may originate from the same tumour, consequently more than one sentinel node is identified.12

Although lymphoscintigraphy is not universally used prior to SLNB, studies support its utilisation.11, 13, 14, 15 Lymphoscintigraphy is a relatively non-invasive imaging modality that allows SN identification by delineating the lymphatic drainage within the axilla. By employing lymphoscintigraphy, accurate topographic co-ordinates are achieved and skin demarcation of the underlying SN is made possible.13 Respondents in favour of performing lymphoscintigraphy prior to SLNB, argue that lymphoscintigraphy serves as a “road map” for the surgeons as it provides an insight to the total number, location and lymphatic pathways of the SNs.11, 16, 17 Lymphoscintigraphy directs surgery towards a more targeted approach, limiting the extent of the dissection hence reducing patient morbidity.13, 18, 19

There is ample evidence that SN visualisation rates (75–100%) in lymphoscintigraphy are encouraging when using optimal technique.20, 21, 22 Nevertheless, certain patient-related and tumour-related factors are consistently reported to impede visualisation of the sentinel node/s on imaging.17, 23, 24, 25, 26, 27, 28, 29 Age24, 28, 29 and obesity (body mass index, (BMI)>30),26, 28 significantly compromise the success of lymphoscintigraphy since the SNs may undergo fatty degeneration reducing the tracer uptake.23, 28 The success of lymphoscintigraphy is also hampered by the tumour size and grading. As the SNs that tend to harbour metastases increase, their ability to retain the radioactive tracer significantly drops, hence metastatic involvement of nodes is significantly correlated to lymphoscintigraphy failure.25, 27, 28, 29, 30

Rempp1 highlighted the diagnostic value of lymphoscintigraphy in SLNB by emphasising the possible variation in the lymphatic drainage routes of the axilla such as: the superficial pectoral, subscapular, supraclavicular and infraclavicular, lateral and central groups. Imaging proves to be fundamental in alerting the surgeon to multiple lymphatic drainage routes and/or to unusual extra-axillary drainage patterns such as internal mammary (IM) drainage.31, 32

Critics of lymphoscintigraphy argue that imaging does not influence the management of breast cancer where the lymphatic drainage is relatively confined to the axilla.16, 26 Several researchers have opposed the use of lymphoscintigraphy on the basis that no valuable diagnostic information is obtained as surgical decisions may be performed intra-operatively using a combination of the blue dye and the gamma probe techniques.9, 33 The blue dye technique is administered prior to the commencement of SLNB and allows the visual confirmation of lymphatic pathways from the tumour site to the SN.34 Proponents of the blue dye technique comment on its cost-effectiveness and accuracy in localising the SNs,35 yet this comes at the expense of life-threatening anaphylactic reactions reported in 1–3% of cases.36 In contrast, the hand-held gamma probe carries no reactions and is relatively safe, apart from the small radiation dose delivered when administering the tracer.37 Gamma probe-guided surgery facilitates surgical exploration by detecting the SN location through the intact skin and prior to the initial incision, hence minimizing tissue disruption.29, 38 By simultaneously combining both blue dye and gamma probe techniques, the SNs identification rates may reach >98%.14, 29

In Malta, the use of lymphoscintigraphy prior to SLNB was introduced during the previous two years. The purpose of this study was to determine the clinical role of lymphoscintigraphy in the visualisation of the sentinel node/s prior to SLNB. This study involved correlating the number of reported SNs identified by lymphoscintigraphy to that revealed by the histology report in order to investigate whether lymphoscintigraphy can predict the operative findings.

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Method 

Ethical approval was obtained from the University of Malta Research and Ethics Committee (UREC ref. no: 077/2010) and permission was obtained from the Imaging Department, Pathology Department and Data Protection Office of the hospital from where the data was collected.

The inclusion criteria involved pre- and post-menopausal females diagnosed with breast cancer between May 2009 and December 2010 who underwent lymphoscintigraphy imaging at the Nuclear Medicine Unit followed by SLNB at the General Public Hospital in Malta. Candidates with known multifocal and multicentric carcinomas of the breast, clinical involvement of the axilla (palpable axillary nodal metastases) and those with a history of previous surgery at the affected breast or axilla, were excluded. The risk of sampling bias, prompted the researchers to assume a consensus approach. This was achieved by including the total population of consecutive patients who satisfied the inclusion criteria, from the commencement of the biopsy procedure in Malta until the collection of the data.

During this period, 55 female patients diagnosed with breast cancer were initially seen at the Nuclear Medicine Unit for the cutaneous (subdermal) administration of 15–25MBq of technetium-99m nanocolloid within the areolar margin of the tumour-bearing quadrant. Immediately following the injection, the patients were instructed to apply light-pressured strokes to stimulate the lymphatic drainage towards the axilla and facilitate uptake of the tracer.11, 26 Pre-operative lymphoscintigraphy imaging was performed between 1 to 2h following the tracer administration. Anterior, anterior oblique and lateral erect lymphoscintigrams were obtained in the static mode. A successful lymphoscintigram consists of the demonstration of the injection site together with the visualisation of at least 1 SN6 (Fig. 1). The full set of images was made available to the surgeons prior to the SLNB.

  • View full-size image.
  • Figure 1 

    (a) A schematic representation of a female patient during lymphoscintigraphy. (b) A successful lymphoscintigram in anterior oblique view. Key: IS, injection site; SN, sentinel node.45

Once the SN was visualised on lymphoscintigraphy, the patient’s chest was silhouetted with the use of a radioactive cobalt-67 contour wire and a cobalt-67 pen was used to facilitate the identification of the surface location of the sentinel node (Fig. 2). The skin overlying the SN was marked by a skin marker to visually direct the surgeon to the node. All patients underwent SLNB followed by tumour resection and partial or total back-up ALND. Identification and retrieval of SNs during surgery was always carried out using an intra-operative gamma probe occasionally complemented by the methylene blue dye technique, the choice of which was left at the discretion of the operating surgeons. During surgical exploration the SN was defined as the “hot” node (tenfold the normal background radiation count on the gamma probe) and/or the stained blue node.11, 26 A successful SLNB is defined as the identification and excision of at least 1 SN.33 The nodes were sent to pathology for a histological evaluation and were examined by Haematoxylin and Eosin (H&E) staining at 2mm intervals.

A data checklist was considered the most appropriate data collection tool for the purpose of the study and was designed to include the following items: the age of the patient, the success or failure of lymphoscintigraphy in the visualisation of the SN, the number of visualised SNs by lymphoscintigraphy, the corresponding number of identified SNs during histological evaluation and the metastatic involvement of the nodes. The research tool was tested for validity by presenting it to two experts in the field (average content validity index, (CVI) 0.85) and the reliability of the checklist was estimated by the inter-rater approach whereby two raters reported a similarity of 1.00. The checklist was also pilot-tested prior to the actual data collection.

Data was analysed using the Statistical Package for the Social Sciences software (SPSS, version 17.0). Data analysis included the Pearson correlation coefficient test, the Chi-square test and the 2-Tailed Independent Sample t-test. All statistical measures were considered significant at the 95% confidence interval (p≤0.05).

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Results 

The sample population comprised of female patients whose ages ranged from 29 to 81 years (mean age, 58.35 years).

A total of 66 axillary SNs were visualised on lymphoscintigraphy in 55 patients (range, 0–2). In contrast, 105 individual SNs were surgically harvested during SLNB in 52 patients (range, 0–9). The Pearson Correlation Co-efficient (0.27) demonstrated a positive but weak correlation (p≤0.05) between the number of SN/s visualised on lymphoscintigraphy and the actual number of SN/s identified during SLNB. Lymphoscintigraphy accurately predicted the number of surgically identified SNs in 50.91% of cases (28/55). In 38.18% of cases (21/55), the intra-operatively biopsied SNs outnumbered the SNs that had been predicted on lymphoscintigrams whereas in 6 patients (10.91%) lymphoscintigraphy depicted more SNs than those found during axillary exploration.

A minimum of 1 sentinel node was visualised on lymphoscintigraphy in 52 out of 55 patients, with an identification rate of 94.5%. A single SN was visualised in 38 patients (69.1%), 2 SNs were visualised in 14 patients (25.4%) whilst the remaining 3 patients (5.5%) had neither visualisation nor identification of the SN during lymphoscintigraphy and during the biopsy, despite the use of the gamma probe and/or the blue dye techniques.

The Chi-square test showed that successful lymphoscintigraphy was highly predictive (100%) (p≤0.001) of a successful SLNB as all 52 patients proceeded to have a successful SN identification during SLNB.

Factors that contributed to non-visualisation of the SN on lymphoscintigraphy such as patient age and metastastatic involvement of nodes were analysed using the t-test and the Chi-square test respectively. Metastasis to the SNs was found in 12 patients (21.8%) whilst metastasis within the ALNs was found in 10 patients (18.2%). There was a significant statistical association (p≤0.05) between lymphoscintigraphic failure and metastatic sentinel and axillary node involvement. In contrast, no effect of patient age on the success rate of lymphoscintigraphy was found. The 2 Tailed-Independent Sample t-Test was used to compare the mean age of patients with successful SN visualisation to those who had no SN visualisation on lymphoscintigraphy. The mean age of patients of the two groups was not considered to be significantly different (p≥0.05).

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Discussion 

With the introduction of the SN concept, breast cancer management has dramatically evolved towards minimally invasive approaches.39 The SLNB is a technique incorporating a multi-disciplinary team approach: nuclear medicine, surgical oncology and pathology departments. A definite technical “learning curve” exists before the personnel become proficient in SLNB which may be improved when lymphoscintigraphy is repeatedly performed.11, 26

Successful SN visualisation on lymphoscintigraphy in this first Maltese study correctly predicts (p≤0.001) the intra-operative identification of SNs during SLNB. These findings corroborated those of previous studies where the concordance between successful lymphoscintigraphy and SN identification during the biopsy was 100%.31, 40, 41 Contrariwise, the experiences of Rousseau et al.,27 and Soran et al.,28 discredit this concept and report no significant difference (p>0.05) between successful imaging and SLNB success.

It is recognised that unsuccessful lymphoscintigraphy does not necessarily forecast SLNB failure.31, 32 McMasters et al.,16 and Wang et al.,42 document that negative SN imaging is a poor predictor of SLNB failure because in the majority of cases (92.1% and 90.9% respectively) the SNs were subsequently still retrieved by the gamma probe and/or the blue dye techniques. This finding has led McMasters et al.,16 to believe that the routine use of lymphoscintigraphy is not justified. However, it is important to note that variations in both injection and imaging techniques were key factors in the report by McMasters et al.16 Not surprisingly, the peritumour injection technique that was adopted in these studies is not the currently preferred one as argued by Duchaj et al.43 The cutaneous (subdermal) application of the tracer within the tumour-bearing quadrant is favoured and is the one used in the local study.

The clinical significance of lymphoscintigraphy remains controversial as there is evidence that it should be put aside since it is not associated with improvements in the retrieval of SNs.16, 33 Mathew et al.,33 questioned the contribution of lymphoscintigraphy in breast cancer by blinding surgeons from the lymphoscintigraphic results, hence eliminating the bias existing before the commencement of SLNB. The authors concluded that lymphoscintigraphy is not an essential prerequisite since 99% of SNs were successfully retrieved when no reference to lymphoscintigrams was made and only 3% of patients had further nodes identified after reviewing the lymphoscintigrams. However, in the study by Mathew et al.33 it appears that the surgeons excelled in the SLNB technique and perhaps had bypassed the technical “learning phase” where the contribution of lymphoscintigraphy is imperative,26 – this is in contrast to the Maltese study where the SLNB was at its early stages and the staff were still being trained.

Non-visualisation of SNs during lymphoscintigraphy is commonly experienced. Several factors such as increased age, obesity, pendulous breasts and metastastatic SNs and ALNs have been proposed as factors that may compromise the success of SN lymphoscintigraphy.17, 24, 28 The visualisation of the SN on lymphoscintigraphy is also hampered by tumour-related parameters such as tumour size (>20mm), grading and location.25, 28 Furthermore, the dose and particle size of the tracer, the injection site and technique may all influence visualisation of the SNs during lymphoscintigraphy.26, 33

The current Maltese study reveals a significant statistical association (p≤0.05) between lymphoscintigraphic failure and metastatic sentinel and axillary node involvement. As the number of axillary nodes (including the SN) that harbour metastases increase, their ability to retain the tracer significantly decreases, hence the success rate of lymphoscintigraphy drops when a SN is mestastatically involved.25, 27 In fact, 2 out of the 3 patients (66.67%) who experienced lymphoscintigraphy failure, were histologically diagnosed with Grade II and Grade III invasive ductal carcinoma – the one having Grade III carcinoma was noted to have metastases in all 25 axillary nodes. The Maltese study concurred with Brenot-Rossi et al.,25 who reported a 50% increased risk of lymphoscintigraphic failure in the presence of >4 metastatically invaded axillary nodes. In fact 63.3% of patients who had no SN visualisation in the study by Brenot-Rossi et al.,25 were found to have positive SNs and ALNs for metastases.

On the other hand, patient age was not a significant (p≥0.05) negative predictor of SN visualisation in the Maltese study. Quite unexpectedly, the mean age range of patients with no visualised sentinel nodes (56.67) was lower than that of patients who had successful SNs visualisation (58.44). These results do not agree with the findings of Goyal et al.,26, Rousseau et al.,27 and Soran et al.,28 who established that a higher patient age increases the incidence of failed lymphoscintigraphy. This may be attributed to the fact that in the Maltese study, the sample of participants with no SN visualisation was limited to only 3 patients. On the other hand, similar findings were reported by Haigh et al.,23 specifying that age is a poor predictor of the non-visualisation of SNs on lymphoscintigraphy.

On the basis of the results presented, it is clear that there is a significant association (p≤0.05) between the number of SNs visualised on lymphoscintigraphy and the number of SNs identified intra-operatively. Although a positive relationship has been established (Pearson coefficient, 0.27), variations in the visualised and identified number of sentinel nodes still remain. In fact, lymphoscintigraphy accurately predicted the number of surgically identified SNs in only 50.91% of cases (28/55). These results agree with the findings of Teal et al.,44 who reported a 47% concordance between the visualised and the identified SNs during the biopsy. Teal et al.,44 observed that in 43% of the cases where the lymphoscintigraphic number was not predictive, the number of intra-operatively harvested SNs was underestimated as more SNs were biopsied than visualised, a finding which relates to the Maltese study’s findings (38.18%).

Possible explanations for the discrepancies in the SN numbers in the Maltese study may be due the fact that a visible single node biopsied during surgical exploration proved to be two nodes on the histopathological analysis.33 Moreover, one of the surgeons utilised both the blue dye and intra-operative gamma probe techniques during SLNB, as a result all the sentinel nodes identified as radioactive, stained blue or both were removed for histological evaluation. Thus, although lymphoscintigraphy exhibits usefulness in ensuring intra-operative identification success, it may not accurately predict the number of SNs that need harvesting during the biopsy.

The main limitation encountered within the Maltese study was the assumption that radiographers working at the Nuclear Medicine unit had bypassed the “learning curve” involved in the accurate skin demarcation of the sentinel node site during lymphoscintigraphy. Likewise, it was assumed that the performing surgeons had the same level of expertise in the SLNB. Another limitation was the availability and accuracy of the patient records due to the retrospective nature of the current study.

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Conclusion 

This study ascertained the diagnostic value of lymphoscintigraphy in the identification of the SNs during SLNB, as the SNs were intra-operatively identified in 100% and 0% of cases with successful and unsuccessful lymphoscintigraphy respectively. Considering that successful imaging effectively assures SN identification, it may be deduced that lymphoscintigraphy is an integral adjunct to SLNB.

Additionally, it offers an insight to the lymphatic drainage, location and number of SNs although it does not accurately predict the number of SNs that may need to be harvested during SLNB. Its implementation also allows the surgeons to tailor incisions at the sentinel node site, hence reducing the invasiveness of SLNB.19 The absence of metastatically involved SNs and ALNs, were associated with a high success rate of the intra-operative SN identification. Patient age did not affect the success rate.

On the basis of the findings of this preliminary evaluation of the introduction of the SLNB procedure in Malta, it appears to be best practice to perform routine lymphoscintigraphy using the cutaneous (subdermal) peri-areolar approach prior to SLNB especially during its early stages when the staff, as in this case, have not yet reached the top of the “learning curve” of the technique.

At present, there is no consensus on the optimal approach of lymphoscintigraphy in breast cancer.15, 22, 43 More studies specifically designed to standardise the protocol of lymphoscintigraphy in terms of the choice and dose of radiopharmaceutical, the technique and site of injection, patient positioning and early versus late imaging, are warranted.

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PII: S1078-8174(11)00140-4

doi:10.1016/j.radi.2011.11.003

Radiography
Volume 18, Issue 1 , Pages 9-14, February 2012

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