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 Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 30  |  Issue : 2  |  Page : 564-571

Nodal ratio and number ofdissected nodes in breast cancer patients with inadequate axillary dissection


1 Clinical OncologyDepartment, Menoufia University, Menoufia, Egypt
2 Radiation Oncology Department, National Cancer Institute, Cairo, Egypt

Date of Submission28-Sep-2016
Date of Acceptance11-Jan-2017
Date of Web Publication25-Sep-2017

Correspondence Address:
Ahmed A Hussein
Department of Radiation Oncology, National Cancer Institute, Cairo, 11796
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.215466

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  Abstract 

Objective
The aim of this study was to evaluate the prognostic significance and to define the optimal cutoff points of nodal ratio and number of dissected nodes in node-positive and node-negative breast cancer patients, respectively, who underwent inadequate axillary lymph node dissection(ALND).
Background
The absolute number of involved axillary lymph nodes(LNs) is considered the most important prognostic factor in breast cancer. Over the last decade, several studies indicated that the lymph node ratio(LNR) might predict outcome better than the number of positive LNs.
Patients and methods
This retrospective study included 200 women with invasive breast cancer. GroupI included node-positive cases with inadequate ALND; groupII included node-positive cases with adequate ALND; groupIII included node-negative cases with inadequate ALND; and groupIV included node-negative cases with adequate ALND. Receiver operating characteristic curve was used to identify cutoff points of LNR in each of the node-positive groups, and number of dissected nodes in node-negative patients, classifying the patients into low-risk and high-risk groups.
Results
Optimal LNR cutoff points classifying node-positive patients into low-risk and high-risk groups were 0.44 for groupI and 0.40 for groupII with statistically significant differences in disease-free and overall survival. There were no statistically significant survival differences between groupsIII and IV. The cutoff point of six dissected nodes classified the node-negative patients into low-risk and high-risk groups with statistically significant differences in disease-free and overall survival.
Conclusion
LNR could be incorporated into the staging of breast cancer patients, especially those with inadequate axillary dissection. LNR cutoff points of 0.44 and 0.40 can be used to classify node-positive patients with inadequate and adequate axillary dissection, respectively, into low-risk and high-risk groups. For node-negative patients, oncologists can be satisfied with a number of dissected nodes as low as seven axillary LNs.

Keywords: breast cancer, inadequate axillary lymph node dissection, lymph node ratio


How to cite this article:
Abd El-Bary NM, Tawfik EA, Abd El-Ghany AE, Shaltout EA, Hussein AA. Nodal ratio and number ofdissected nodes in breast cancer patients with inadequate axillary dissection. Menoufia Med J 2017;30:564-71

How to cite this URL:
Abd El-Bary NM, Tawfik EA, Abd El-Ghany AE, Shaltout EA, Hussein AA. Nodal ratio and number ofdissected nodes in breast cancer patients with inadequate axillary dissection. Menoufia Med J [serial online] 2017 [cited 2018 Apr 22];30:564-71. Available from: http://www.mmj.eg.net/text.asp?2017/30/2/564/215466


  Introduction Top


Breast cancer ranks as the first malignancy affecting women, accounting for 29% of cancer in the female population. Breast cancer is second only to lung cancer as a cause of cancer-related death in women[1].

Metastasis to the axillary lymph nodes(LNs) is a key indicator of prognosis in breast cancer[2]. The AJCC TNM staging system for breast cancer emphasized the importance of the absolute number of positive nodes in the N classification for staging breast cancer: pN1 disease indicates 1–3 positive axillary nodes, pN2 denotes 4–9 positive nodes, and pN3 is defined as 10 or more positive nodes[3].

The potential issue of using the absolute number of affected nodes for staging is the dependence upon the overall number of nodes examined. In other words, three positive nodes out of a total of five examined have a different implication compared with three positive nodes out of 10 examined[4].

Although some studies noted that six nodes were the minimum number of nodes needed to adequately assess the axilla[5], it is generally accepted that greater than 10 LNs are required[6]. When 10 or less nodes are removed, there is a greater probability that some patients with four or more positive nodes will be misclassified as having 1–3 positive nodes. In other words, patients are potentially understaged[7].

An increasing dilemma for clinicians is whether to give patients with 1–3 N+postmastectomy radiation therapy, particularly if a patient had undergone inadequate axillary dissection. When lesser than or equal to 10 nodes are removed, there is a greater probability that some patients with four or more positive nodes will be misclassified as having 1–3 positive nodes[8].

In these cases with few nodes removed, patients cannot be classified as having pN3 disease, which can affect comparisons between institutions in which the practices of axillary dissection differ. To improve the prognostication system, one would intuitively take not only the number of positive LNs but also the number of nodes examined into account[9].

Several studies have examined the concept of the lymph node ratio(LNR), defined as the number of positive LNs over the number of LNs removed, as a potential prognostic factor in breast cancer and suggested that it may be an alternative and possibly a better indicator of axillary tumor burden and consequently disease prognosis compared with pN staging[10],[11],[12],[13],[14].

Vinh-Hung etal. [12] defined optimal cutoff points for LNRs and divided the population into those at low-risk(≤0.20), moderate risk(>0.2 and≤0.65), and high-risk(>0.65). The LNR groups had significantly different survival rates and were more accurate compared with pN status for predicting survival.

Many studies have reported a strong association between the extent of axillary dissection and the number of positive nodes and an association with survival, both in node-negative and node-positive patients[15]. Conversely, one study described worse outcomes with the removal of more LNs[16].

A retrospective study of 833 node-negative breast cancer patients who underwent mastectomy and 1094 node-negative patients who underwent breast-conservation therapy showed that the recovery of less than 10 LNs in LN-negative patients who underwent mastectomy resulted in a 10–15% decreased long-term disease-free survival(DFS) rate compared with patients who had a more extensive axillary assessment. However, the number of LNs examined did not have an impact on the DFS rate in a contemporary cohort of patients who underwent breast-conservation therapy, which included radiation[17].

Encouraged by these results and the fact that inadequate axillary dissection(i.e.,excision of 1–9 axillary LNs) is a frequently encountered situation in our daily practice, we conducted this study aiming to evaluate the prognostic significance and to define the optimal cutoff points of nodal ratio and number of dissected nodes in node-positive and node-negative breast cancer patients, respectively, who underwent inadequate axillary LN dissection.


  Patients and Methods Top


Patients

This retrospective study was conducted at the Clinical Oncology Department, Menoufia University, for patients with invasive primary breast cancer who underwent inadequate axillary dissection from January 2009 to December 2013.

This study was approved by the Ethical Committee of Faculty of Medicine, Menoufia University.

Eighty-eight patient files with inadequate axillary dissection were recognized, 50 of which were for node-positive patients and 38 for node-negative patients. Amatched group of 112patients with adequate axillary dissection was selected: 70 were node-positive and 42 were node-negative. The total number was 200patients, representing the study population.

Eligibility criteria

Female patients with histologically proven primary invasive breast carcinoma who underwent a curative breast cancer surgery including axillary LN dissection, and aged from 18 to 70years old were included in the study.

Exclusion criteria

Exclusioncriteria were as follows: metastatic breast cancer at the time of diagnosis, incomplete data from medical records, bilateral breast cancer, or diagnosis synchronous with malignancy other than breast cancer.

Methods

Patient files were searched for the following information for each patient: patient characteristics, diagnostic methods, histological features of the tumor, including immunohistochemistry, number of dissected and positive LNs, LNR, treatment details, recurrence data, and survival. The endpoints for the survival analyses were DFS and overall survival(OS).

Definitions

Inadequate axillary dissection was defined according to NCCN guidelines 2015 as the total number of axillary LNs excised ranging from one to nine LNs. LNR was defined as the number of positive LNs over the number of LNs removed.

Statistical analysis

Survival functions were estimated by applying the method of Kaplan and Meier. The log-rank test was used to assess the significance of unadjusted differences in survival. Exploration of variables for their independent prognostic effect on survival was carried out using the multivariate stepwise Cox's proportional regression hazard model. Receiveroperating characteristic(ROC) curve was used to identify the cutoff points of nodal ratio and number of dissected nodes. Atwo-tailed P value of less than 0.05 was considered statistically significant. All statistical evaluations were carried out using the computer statistical package(IBM SPSS statistics for Windows, version22.0; IBM Corp., Armonk, NewYork, USA).


  Results Top


Two hundred patients were considered eligible for the analysis; none of them underwent a sentinel LN procedure.

[Table1] depicts patient, disease, and treatment characteristics. For the entire cohort, the median follow-up period was 47months, the mean age was 47years, and 78% of patients were older than 40 at the time of diagnosis. In this series, 56% of patients had pT2 disease, 40% of patients were node-negative, and 31% had a pN1 disease. Invasiveduct carcinoma was found in 89.5% of the cases, 87% of cases were of gradeII, and 74% of cancers were hormone positive, whereas only 17.5% had Her2 overexpression.
Table 1: General characteristics of the patients

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Radical surgery was performed in all cases; 77% of the cases underwent modified radical mastectomy. The number of dissected nodes ranged from 1 to 40, and the mean was 14.3. Overall, 85% received chemotherapy, 71.5% received adjuvantradiotherapy(RTH), and 74% received adjuvant hormonal treatment, whereas only 6% received adjuvant trastuzumab.

Lymph node ratio for node-positive patients

GroupsI and II were separately tested for the cutoff points of nodal ratio, according to which the patients can be stratified into high-risk and low-risk groups.

For groupI, node-positive patients with inadequate axillary dissection(n=50), the cutoff point of nodal ratio was found to be 0.44 with a sensitivity of 70.6% and a specificity of 78.8%. The mean DFS for low-risk patients(nodal ratio≤0.44) was 59.6months, compared with 19.5months for the high-risk patients(nodal ratio>0.44) with a highly significant P value of less than 0.001. Kaplan–Meier curve for DFS in this group is shown in [Figure 1]. The mean OS for the low-risk group was 72.2months, compared with 62.1months for the high-risk group(P=0.01). OS curve is shown in [Figure 2]. The nodal ratio was found to be an independent adverse prognostic factor for DFS and OS in the multivariate analysis for this group of patients[Table2] and [Table3].
Figure 1: Kaplan-Meier curve for disease-free survival in relation to nodal ratio in group I (n = 50).

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Figure 2: Kaplan–Meier curve for overall survival in relation to nodal ratio in group I (n = 50).

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Table 2: Multivariate analysis of factors affecting disease-free survival among node-positive cases inadequately dissected (group I)

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Table 3: Multivariate analysis of factors affecting overall survival among node-positive cases inadequately dissected (group I)

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For groupII, node-positive patients with adequate axillary dissection(n=70), the nodal ratio cutoff point was found to be 0.40 with a sensitivity of 83.3% and a specificity of 92.3%. The mean DFS for low-risk patients(nodal ratio≤0.40) was 67.3months, whereas for high-risk patients(nodal ratio>0.40) it was 19.6months(P<0.001). The mean OS for low-risk patients was 98.2months, compared with 68.7months for the high-risk patients(P<0.001). Kaplan–Meier curves for DFS and OS in this group are shown in [Figure 3] and [Figure 4]. The nodal ratio was found to be an independent adverse prognostic factor for DFS[Table4], but not for OS in the multivariate analysis for this group of patients.
Figure 3: Kaplan-Meier curve for disease-free survival in relation to nodal ratio in group II (n = 70).

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Figure 4: Kaplan–Meier curve for overall survival in relation to nodal ratio in group II (n = 70).

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Table 4: Multivariate analysis of the factors affecting disease-free survival among node-positive cases adequately dissected (group II)

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The number of dissected nodes in node-negative patients in groupsIII and IV

There was only a marginal difference in DFS and OS between the two groups, with no statistical significance in either of them. The mean DFS for groupsIII and IV was 105.7 and 106.7months, respectively(P=0.57). The mean OS was 103.6months for groupIII and 124.3months for groupIV(P=0.48).

ROC curve was used to identify the optimal cutoff point for the number of dissected nodes among the whole node-negative patients(n=80). The result was six LNs with a sensitivity of 83.3% and a specificity of 91.9%. The mean DFS for low-risk patients(>6 LNs dissected) was 114.4months, whereas for high-risk patients (≤6 LNs) it was 45.6months(P<0.001). The mean OS was 126.7 and 70.4months for low-risk and high-risk patients, respectively(P=0.035). Kaplan–Meier curves for DFS in node-negative patients, according to the cutoff point of six dissected LNs are shown in [Figure 5].
Figure 5: Kaplan-Meier curve for disease-free survival. (DFS) in relation to the number of dissected nodes in node.negative patients (n = 80) (P < 0.001).

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The multivariate analysis showed the number of dissected nodes, according to this cutoff point, to be an independent prognostic factor for DFS together with the ER status[Table5]. However, for OS there were no other significant factors other than the number of dissected nodes in the univariate analysis.
Table 5: Multivariate analysis of the factors affecting disease-free survival among node-negative patients

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  Discussion Top


LNR has been widely demonstrated to be a useful alternative to predict survival in many cancers, including lung[18], colon[19], pancreas[20], bladder[21], and particularly breast cancer. [Table6] shows some recent studies published since 2008 and these studies confirmed the superiority of LNR over the number of involved nodes as an adverse prognostic factor for breast cancer.
Table 6: Recent studies (2008-2013) of ratios of involved nodes in breast cancer

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Lymph node ratio for groupsI and II

Vinh-Hung etal.[12], in their study on 1829 node-positive breast cancer patients from the Geneva Cancer Registry, defined the optimal cutoff points for LNRs and divided the population into those at low-risk(≤0.20), moderate risk(>0.2 and≤0.65), and high-risk(>0.65). The LNR groups had significantly different survival rates and were more accurate compared with pN status for predicting survival[12]. In view of our relatively small sample size, we tried to define a single cutoff point for each of the two node-positive groups to divide patients into low-risk and high-risk groups. This is similar to that reported by Truong et al. [22], who identified a single nodal ratio cutoff point, estimated 0.25, in their study of 4571 node-positive patients.

For groupI, the identified nodal ratio cutoff point of 0.44 lies in the range of the intermediate risk group defined by Vinh-Hung etal. [12](0.21–0.65); our results are consistent with their results. The significance of nodal ratio for this group as an adverse prognostic factor for both DFS and OS is in agreement with the results published by Jayasinghe etal.[14], who reported that LNR predicts survival more accurately when a lower number of LNs is removed. They studied 332patients with node-positive breast cancer and found the nodal ratio to be an independent predictor of 10-year breast cancer-specific survival when 5–15 LNs were removed, but lost its significance when more than 15 LNs were removed[14].

The failure of pN stage to significantly prognosticate DFS in the multivariate analysis in the first group of our study can be attributed to the absence of N3 stage in this group of patients.

Another Egyptian study conducted by Elkhodary etal. [25] included 500patients with node-positive breast cancer. Among them, 93patients had less than 10 LNs dissected. They used the same LNR cutoff points defined by Vinh-Hung etal.[12], and found the LNR together with ER negativity and tumor grade, the only factors to influence DFS in the multivariate analysis. The pN stage in their study was only significant in univariate analysis, which as well supports our results[25]. For OS multivariate analysis, our study showed that LNR was an independent adverse prognostic factor(P=0.03), together with the AJCC stage group, pT stage, pN stage, and extracapsular invasion. Again, this is similar to the results of other published studies, such as those by Elkhodary etal.[25]and Schiffman etal.[23].

In groupII, the identified nodal ratio cutoff point of 0.40 in this group of our study lies in the range of the intermediate risk group defined by Vinh-Hung etal. [12] (0.21–0.65); our results are consistent with their results. However, it is higher than the cutoff point of 0.25 identified by Truong etal.[22]. This difference in the value from that reported by Truong etal. [22] is probably because they did not take into consideration the number of dissected nodes, which ranged in their study from 1 to 50 nodes, whereas this group of our study was made of adequately dissected patients(i.e.,≥10 LNs removed).

This group of our study showed both LNR and pN stage to be significant adverse prognostic factors in the univariate analysis, but not in the multivariate analysis, highlighting that LNR could be more significant when a lower number of LNs are dissected as suggested by Jayasinghe etal.[14]. However, a large population-based study of 25315 Dutch patients conducted by Dings etal. [24] showed that both pN stage and LNR are independent adverse prognostic factors for OS, recommending the incorporation of the LNR as an independent factor in the staging of breast cancer.

Number of dissected nodes for node-negative patients

Our study showed no significant survival differences between the two node-negative groups when the cutoff point of 10 dissected LNs was used. This could be attributed to the confounding effect of systemic therapy observed by Weir etal. [26] in their study on 2278 node-negative breast cancer patients, who found that, for patients not receiving systemic therapy, regional relapse was significantly increased with smaller numbers of nodes removed(P=0.03). There was a trend toward shorter OS with fewer nodes removed(P=0.06). Node-negative patients who received systemic therapy did not have a higher regional relapse rate or shorter OS when fewer nodes were recovered[26].

RTH also can confound the effect of number of dissected nodes on survival, as shown by the study conducted by Salama etal.[17], who examined the cutoff point of 10 dissected nodes in 833 node-negative patients who underwent mastectomy and 1094 node-negative patients who underwent breast-conservation surgery followed by RTH. Their results showed that the recovery of less than 10 LNs in LN-negative patients who underwent mastectomy resulted in a 10–15% decreased long-term DFS rate compared with patients who had a more extensive axillary assessment. However, the number of LNs examined did not have an impact on the DFS rate in a contemporary cohort of patients who underwent breast-conservation therapy, which included radiation[17].

However, another study conducted by Moorman etal. [27] used a cutoff point of 20 dissected LNs and showed that the number of LNs examined was not found to be associated with either 5-year or long-term survival. The proportion of women dying from breast carcinoma was the same(8%) in both groups(those patients with≥20 LNs examined vs. those in whom<20 LNs were examined) and the hazard ratio was 0.98(95% confidence interval, 0.58–1.64), suggesting that it is unlikely that the number of LNs examined is an important prognostic indicator in patients with LN-negative breast carcinoma[27].

When we used the cutoff point of six dissected LNs that was identified using ROC curve, there were significant DFS and OS differences between the low-risk and high-risk patients. Thisis in agreement with the results of Blancas etal.[28], who conducted a retrospective study on 1606 node-negative invasive breast cancer patients and found that resection of less than six LNs in node-negative patients resulted in lower DFS and breastcancer-specific survival in both univariate and multivariate analysis, suggesting that six or more nodes need to be examined at axillary dissection to be confident of a node-negative status.


  Conclusion Top


Our results support the accumulating evidence that LNR could be incorporated into the staging of breast cancer patients, especially those with inadequate axillary dissection. LNR cutoff point of 0.44 can be used to classify node-positive patients with inadequate axillary dissection into low-risk and high-risk groups. LNR cutoff point of 0.40 can be used to classify node-positive patients with adequate axillary dissection into low-risk and high-risk groups. For node-negative patients, oncologists can be satisfied with a number of dissected nodes as low as seven axillary LNs.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table1], [Table2], [Table3], [Table4], [Table5], [Table6]



 

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