Sentinel lymph node biopsy is currently the preferred method of axillary staging for early breast cancer. Delivering high-quality care is a priority for stakeholders in breast cancer management; therefore, having a set of suitable QIs for SLNB is important to guarantee optimal survival rates. Assuring optimal axillary staging can be achieved by practising evidence-based medicine, adhering to protocols, applying QIs and undergoing accreditation with periodical reassessment of the results.
The aim of this study was to evaluate the applicability of a set of novel QIs for SLNB by using our breast cancer centre’s data as a means of exercise. By not limiting our data collection to cross-sectional chart review, but also including a longitudinal review of patients who completed 5 years of post-SLNB follow-up, we were able to measure all 11 criteria. Overall, our SLNB performance complied with almost all the indicators, similar to the first study that reported using these QIs.15
The study by Wells and colleagues15
was also carried out in Toronto, yet neither cohort used the same patient population. However, the content in that research group’s registry limited their study. Both that study and ours described optimal patient selection, proper technique results and adequate compliance with protocols. During the course of our study, we found that some of the QIs required modifications to make their applicability more relevant. For example, correct pathological interpretation of the SLN is important for correct staging, yet it does not depend on the surgical technique per se. Before offering SLNB, cancer centres must secure a trained pathology staff with a pathological evaluation/reporting protocol in accordance with AJCC guidelines. Therefore, having a pathological evaluation protocol and pathological reporting by AJCC guidelines should be reclassified as structural components of the hospital. This is also suggested for the QI regarding protocol for injection of radio-colloid. The remaining QIs allow surgeons to track individual performance, but we also suggest that some of these QIs need more precise definitions and more inclusive target rates because they fall short of what has been published in the literature (). For example, the QI regarding the number of nodes removed should set an upper limit to the number of nodes excised, as studies show no benefit when more than 4 SLNBs are excised. Also, the QI of SLNB performance in ineligible patients requires a clearer definition. There are specific situations in which SLNB is indicated (e.g., mastectomies for high-risk ductal carcinoma in situ [DCIS], prophylactic mastectomies in very high-risk patients, and prior axillary procedures). Given the complex method in which this group of QIs was developed, we suggest the modifications and outline of the personal SLNB registry be done in the same fashion.
Suggested issues for improvement in sentinel lymph node biopsy quality indicators
The only indicator that had results below the suggested target was the percentage of SLNB performance in eligible patients (78.1% v. ≥ 80%). To calculate the percentage, Quan and colleagues9
proposed that only T1 tumours be used, excluding other eligible cases (e.g., T2N0, TisN0). Although SLNB is indicated for most T1 tumours, only 60% of them undergo this type of axillary staging.16
Sentinel lymph node biopsy is feasible and accurate in T1–T3 tumours, and this QI appears to be irrelevant. Higher percentages of T2 or T3 tumours in a surgeon’s series may reflect their case mix rather than a selection bias. In addition, the frequent use of preoperative magnetic resonance imaging (MRI), ultrasonography and fine needle aspiration identifies suspicious axillary nodes, reducing the number of patients eligible for the technique.
In our cohort, the axillary node positivity rate was 20.3% for patients with in situ carcinoma and invasive carcinoma. The expected percentage of positive SLNs in patients with invasive breast cancer ranges from 17% to 35%.17,18
Ideally, this QI should be strictly followed because it speaks of each surgeon’s capacity to select patients appropriately. Higher positivity rates may imply bias in the selection of patients with more advanced disease (e.g., T3N0), and lower rates may be due to a greater proportion of high-risk DCIS or prophylactic mastectomy cases. Stratifying our cohort by tumour size exposed a predominant number of patients with tumours smaller than 2 cm (63.6%) and a substantial proportion of high-risk patients with DCIS (9.3%). Currently, patients undergo additional preoperative work-up (e.g., axillary ultrasound, fine needle aspiration of suspicious nodes, and/or preoperative MRI), which filters the patients with positive nodes before surgery and consequently reduces the probability of finding positive SLNs during surgery.
In terms of the number of nodes removed, our performance also met current standards. In all, 206 (68.7%) patients had 2–4 nodes removed. Studies suggest that the false-negative rate decreases when more than 1 SLN is harvested, yet removing more than 4 nodes provides no additional benefit.19
Therefore, we consider that this particular QI requires a more detailed definition, specifically in setting the upper limit of number of SLNs to remove.
Current evidence in the literature shows that selected cases of micrometastasis may have such a low probability of additional positive non-SLNs that ALND can be avoided without compromising overall survival in patients receiving adjuvant therapy.20
A lower compliance rate in this parameter could be accepted if the MSKCC nomogram14
is applied, but we consider that this QI should also be redefined to take into account the current evidence regarding micro-metastasis and isolated tumour cells.
On subgroup analysis of patients completing 5 years of follow-up (n
= 42), only 1 (2.5%) had axillary recurrence. This analysis may overestimate the actual axillary recurrence rate (ARR). Our whole cohort’s ARR could not be calculated because most surgeries were recently performed. The reported ARR in the literature is 0%–1.4%.21–23
A meta-analysis of 14 959 SLN-negative breast cancer patients followed for a median of 34 months reported an average ARR of 0.3%.24
Lower ARRs have been associated with the following factors: performing SLNB in cancer centres, probably reflecting volume and expertise of the surgeons; using 99mTc-sulfur colloid; using a superficial injection technique; or evaluating the harvested sentinel nodes with hematoxylin/eosin and immunohistochemistry staining.24
In practice, this QI should fluctuate over time, eventually decreasing as more patients complete 5 years of follow-up. Ultimately, the ARR is a strong QI because it directly correlates with the false-negative rate and is the end product of proper patient selection, training and surgical technique.
In our series, patients in whom SLNB was not concurrently performed with primary surgery were those treated for DCIS but who were later found to harbour invasive disease. This QI was suggested without any significant published evidence; despite some authors suggesting that performing primary surgery before SLNB alters the pattern of lymphatic drainage and increases the false-negative rate, others have not shown this relationship to exist.25
Though not included in the set of QIs, postoperative complication rates must be a part of quality assessment because the rationale to use SLNB over ALND is its major impact in reducing morbidity (e.g., surgical site infection, seroma formation, permanent lymphedema, nerve injury, arm weakness, restriction in shoulder mobility).26
Most of these sequelae are difficult to treat satisfactorily, creating impaired function and emotional distress and increasing cost of treatment.27
We propose that shoulder–arm symptoms (e.g., lymphedema, nerve injury, range of motion) be included as a QI. Other less dramatic arm-related symptoms (e.g., nerve damage, limited shoulder movement) should be incorporated because they speak of the surgeon’s skill.
The purpose of using QIs is to improve performance. Bearing in mind that most institutions and individual reporting surgeons are above quality standards, there really is little room to improve. Consequently, this exercise should be carried out to monitor performance. Quality indicators are useful if they can be continuously and easily applied so that necessary measures can be taken promptly. Despite the fact that Wells and colleagues15
and our study show how feasible it is to extract data from an institutional database, we propose that every surgeon do this excersise individually. Cancer registries are usually an asset of large centres, but as SLNB becomes available in private practice settings, these QIs should be accompanied by a structured guide of how to create and maintain a simple, prospective personal SLNB registry.
The quality of SLNB must also be assured on every level of complexity of breast cancer management, including for surgeons with small caseloads. General surgeons practising in rural settings and small hospitals are less likely to perform SLNB.28
In addition, rural regions have only recently validated and adapted SLNB into practice.28
In this setting, these QIs for SLNB will certainly play an important role in improving performance, but achieving benchmarks will take time owing to the limited number of eligible cases. Therefore, it may be necessary for these QIs to be adapted for surgeons with small caseloads, so that the actual progress made is not underestimated. Setting targets well above reality allows for inappropriate, unintended decisions to occur in patient care.
Despite being a highly studied medical topic, breast cancer treatment needs further study to establish standard QIs. In the past, organizations developed quality programs that provided assessment of different aspects of breast care.8,29–32
Participating in these programs implies substantial use of resources and time.32
The generic QIs suggested by these groups reduced SLNB assessment to only measuring percentage of SLNB use in eligible patients, SLNB use in mastectomy for DCIS, and pathology frozen section SLN false-negative rates.33
Other efforts, such as those of the Spanish Society of Senology and Breast Pathology have been more inclusive, focusing on 3 major areas: complexity of care and patient volumes, processes of care and academic activity.32