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  Table of Contents  
Year : 2019  |  Volume : 56  |  Issue : 3  |  Page : 228-235

Prognostic significance of residual nodal burden using lymph node ratio in locally advanced breast cancer after neoadjuvant chemotherapy

1 Department of Breast and Gynecology Oncology, Amrita Institute of Medical Sciences, Kochi, Amrita Vishwa Vidyapeedham, Kerala, India
2 Department of Medical Oncology, Amrita Institute of Medical Sciences, Kochi, Amrita Vishwa Vidyapeedham, Kerala, India

Date of Web Publication19-Jul-2019

Correspondence Address:
D K Vijaykumar
Department of Breast and Gynecology Oncology, Amrita Institute of Medical Sciences, Kochi, Amrita Vishwa Vidyapeedham, Kerala
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijc.IJC_652_18

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 » Abstract 

OBJECTIVE: To investigate the prognostic value of lymph node ratio (LNR) after neoadjuvant chemotherapy (NAC) according to breast cancer molecular subtypes.
METHODS: From 2004 to 2014, patients with definitive surgery after NAC were identified. LNR was calculated for node positive patients who underwent axillary dissection and at least 10 nodes (LNT) were removed. Disease free and overall survivals were analysed using Kaplan-Meier test and compared using log rank test for ypN0-3, LNR categories (LNRC) ≤0.2 (low), 0.21-0.65 (intermediate), >0.65 (high), and single LNR cut-off value.
RESULTS: Of 224 analysed patients: ypN0 72 (32.1%), ypN+ 152 (67.9%). Of 118 LNT ≥10 ypN+ patients LNRC: Low risk 48 (40.7%), intermediate risk 36 (30.5%), high risk 34 (28.8%). Factors significantly different in LNR categories were ypN (P < 0.001); extranodal extension (P < 0.001); present status of patients (P < 0.001); and disease status (P = 0.029). LNRC was inversely associated with 5-year DFS: Low 52.3%, intermediate 40%, and high 12.2% (log rank P < 0.001); and OS: Low 64.4%, intermediate 58.3%, and high 13.6% (log rank P < 0.001). Significant association of LNRC and DFS and OS were demonstrated in TNBC (P < 0.001) and HER2 subtypes (P = 0.045 and 0.005 respectively). A single value of LNR = 0.25 in node positive was found significant for DFS and OS in TNBC (P < 0.001) and Her2+ (P = 0.013 and P = 0.001 respectively) but not for HR+ (DFS: P = 0.132; OS: P = 0.144).
CONCLUSION: Residual nodal disease after NAC analysed by LNRC or LNR = 0.25 cut-off value, is prognostic and can discriminate between favourable and unfavourable outcomes for TNBC and Her2+ breast cancers.

Keywords: Lymph node ratio categories, lymph node ratio single cut-off value, molecular subtypes, neoadjuvant chemotherapy, survival, ypN

How to cite this article:
Agarwal R, Philip A, Pavithran K, Rajanbabu A, Goel G, Vijaykumar D K. Prognostic significance of residual nodal burden using lymph node ratio in locally advanced breast cancer after neoadjuvant chemotherapy. Indian J Cancer 2019;56:228-35

How to cite this URL:
Agarwal R, Philip A, Pavithran K, Rajanbabu A, Goel G, Vijaykumar D K. Prognostic significance of residual nodal burden using lymph node ratio in locally advanced breast cancer after neoadjuvant chemotherapy. Indian J Cancer [serial online] 2019 [cited 2021 Dec 5];56:228-35. Available from: https://www.indianjcancer.com/text.asp?2019/56/3/228/263043

 » Introduction Top

In breast cancer, axillary lymph node (LN) involvement upstages the disease, is prognostic and it plays a major role in deciding the treatment strategy.[1] There is a direct relation between the risk of recurrence and number of positive nodes, while overall survival is inversely related to the number of positive nodes.[2],[3]

TNM staging does not take into account the total number of LNs retrieved. Studies have shown improved survival with more extensive nodal dissection in both node-negative and node-positive breast cancer.[4],[5] However, due to the varying effects of NACT on nodal status, the number of LNs detected after neo-adjuvant chemotherapy (NACT) is significantly lower than in patients undergoing upfront surgery.[6],[7],[8] This often leads to underestimation of true axillary lymph node status in these patients. Therefore, more accurate methods for assessment of axillary lymph node status are required.

Lymph node ratio (LNR) is defined as the proportion of positive lymph nodes over the total number of nodes excised. LNR has been shown to provide prognostic information with respect to disease free survival (DFS) and overall survival (OS).[9],[10],[11],[12]

In this study, we aimed to investigate the prognostic value of LNR in LABC patients receiving NAC followed by definitive surgery with adequate axillary dissection (defined as ≥10 lymph nodes) across various breast cancer intrinsic subtypes. We also aimed to investigate whether LNR can provide any additional prognostic information along with pathological nodal (ypN) stage after an adequate axillary dissection.

 » Methods Top


This is a single institution, retrospective review of patients with LABC who underwent NAC, followed by definitive surgery during the years 2004-2014 in the Department of Breast and Gynaecology Oncology. The study was conducted after obtaining approval from the institutional review board.

[Table 1] depicts the inclusion and exclusion criteria used in the study and the patient, tumor and treatment specific characteristics collected from the electronic medical record for each patient.
Table 1: Inclusion and Exclusion criteria and Patient, tumor and treatment specific characteristics recorded

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Based on total number of lymph nodes (LNT) removed, patients were dichotomized into two groups: <10 and ≥10 LNT groups. Lymph node ratio (LNR) was defined based on the study by Vinh-Hung et al.[11] LNR was calculated and analysed only for patients with ≥10 axillary lymph nodes removed and patients were divided into three risk groups: LNR ≤ 0.20 (low), ≥0.21 to ≤0.65 (intermediate), >0.65 (high).

Based on the pathological nodal stage the entire cohort was divided into node negative and node positive subcohorts. Clinical tumor and treatment specific characteristics were compared for both the subcohorts.

Follow-up and survival endpoints

After initial diagnosis, patients were followed up once every 3-6 months. The end points of this study were disease-free survival (DFS) and overall survival (OS). Locoregional recurrence was defined as “pathological proven recurrence in the ipsilateral chest wall, supraclavicular and infraclavicular areas, axilla and internal mammary region.” Distant metastasis was defined as “recurrence at any other site other than those defined as locoregional, subjected to confirmation by imaging studies and pathological examination when indicated.” DFS was defined as “the time period from diagnosis till the date of first recurrence (locoregional and/or distant) or last follow up.” OS was defined as “the time period from diagnosis till the date of death (both breast cancer and non-breast cancer related deaths) or last follow up.” The present status of patients was defined according to their status on last follow up (30th April 2017) as alive no disease (AND), alive with disease (AWD), died of disease or other causes (DOD), and lost to follow up (LFP).

Statistical analysis

The Kaplan-Meier method was used to calculate the survival rate and plot the survival curves. Differences in survival curves were examined using log-rank test. A multivariate Cox regression model was performed using the stepwise method, and significant variables in univariate analysis (P < 0.05) were entered into a multivariate Cox regression model. All analysis performed using IBM SPSS for Windows, version 20, and a value of P < 0.05 was considered to indicate statistical significance.

 » Results Top

Baseline characteristics

Out of a total 1121 LABC patients during the study period, 423 patients who underwent definitive surgery after NAC were identified from hospital medical records. Only 224 patients met the inclusion criteria for the analysis [Figure 1].
Figure 1: Consort Diagram

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The mean age at diagnosis was 48.6 years (Range 25-81 years). Out of 224 patients, 72 (32.1%) were pathologically staged as node negative (ypN0) and 152 (67.9%) as node positive (ypN+) [Table 2]. Specifically 62 (27.7%) were classified as ypN1, 54 (24.1%) as ypN2 and 36 (16.1%) as ypN3. Median number of lymph nodes removed at axillary dissection was 15 (Range 1-44) in the ypN+ cohort versus 12 (Range 1-31) in the ypN0 cohort (P = 0.003). Median number of positive lymph nodes was 5 (Range 1-38) in ypN+ cohort. In the ypN0 cohort, 20/72 (27.8%) patients and in ypN+ cohort 34/152 (22.4%) patients had less than 10 total lymph nodes removed (p = 0.235). LNRs in the ypN+ cohort ranged from 0.03 to 1 with a mean of 0.42 and median of 0.3. Out of the 118 ypN+ patients in whom ≥10 LNs were dissected, LNR was calculated. 48 (31.6%) patients were in the low-risk, 36 (23.7%) in the intermediate- risk and 34 (42.1%) in the high-risk group.
Table 2: Patients, tumors, treatment specific characteristics and outcome in ypN0 and ypN+ cohort

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[Table 2] summarizes the comparison of patient-, tumor- and treatment-specific characteristics between the ypN0 and ypN+ cohorts. Both the cohorts were comparable for the age and the menstrual status of the patients. 58.3% patients had N1 disease in ypN0 cohort while in ypN+ cohort 44.1% patients had N2/N3 disease (p = 0.034). The most common intrinsic subtype in both cohorts was triple negative. 92.9% patients had ductal carcinoma (92.1% in ypN+ and 94.4% in ypN0 cohort; P = 0.329). Both the cohorts were comparable in the type of treatment received that is: Type of NACT regimen (p = 0.076), number of NACT cycles before the definitive surgery (p = 0.497) and the type of definitive surgery (p = 0.160). In both the cohorts, the most common NACT regimen given was anthracyclin and taxane, based in 64.3% patients (91.5% in ypN+ and 86.1% in ypN0 cohort; P = 0.076). Modified radical mastectomy was done in 89.7% of the patients (65.8% in ypN+ and 61.1% in ypN0 cohort; P = 0.160). Lympho-vascular space invasion (LVSI) was present in 43.8% patients (54% in ypN+ versus 22.2% in ypN0 cohort; P < 0.001).

Patients' outcome

The median duration of follow up was 61 months (Range 3-151 months). In all, 62 (27.7%) patients died during study period: 10 (16.1%) in the ypN0 cohort and 52 (83.9%) in the ypN+ cohort; 4 patients died due to Adriamycin-induced toxicity (1 in ypN0 and 3 in ypN+). Out of the 153 patients who were alive, 131 are alive with no disease (AND) (54 in ypN0 and 77 in ypN+ cohort) and 22 are alive with disease (AWD) (6 in ypN0 and 16 in ypN+ cohort). A total of 80 patients had disease recurrence: 17 in the ypN0 and 63 in the ypN+ cohort. Four patients had progressive disease and all of them had ypN+ disease [Table 3].
Table 3: Characteristics and outcome in LNR categories

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The nodal stage inversely correlated with 5 and 10-year DFS respectively: 74.9% and 72.5% (ypN0), 52.7% and 36% (ypN+), more specifically 65.5% and 53.4% (ypN1), 53% and 40.9% (ypN2) and 26.3% and 6.6% (ypN3), log rank P < 0.001 [Figure 2]a. Nodal stage was also inversely correlated with 5 and 10-year OS respectively: 87.1% and 81.5% (ypN0), 60.2% and 49% (ypN+), more specifically 78.4% and 66% (ypN1), 71.3% and 47.2% (ypN2) and 35.2% and 16.1% (ypN3), log rank P < 0.001 [Figure 2]d. These differences in DFS and OS were not only significant when comparing ypN0 to ypN+ categories, but also significant when comparing ypN1, ypN2 and ypN3 categories (log rank P < 0.001) [Figure 2]a and [Figure 2]d.
Figure 2: Comparison of 5-year disease-free survival (DFS) and overall survival (OS) among all node positive patients, by different ypN nodal stage, lymph node ratio category (LNRC), and single LNR cut-off value. (a) DFS and ypN staging; (b) DFS and LNRC; (c) DFS and single LNR value 0.25; (d) OS and ypN staging; (e) OS and LNRC; (f) OS and single LNR value 0.25

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Like the ypN stage, LNR category (LNRC) was found to have an inverse correlation with 5 year DFS: Low 52.3%, intermediate 40%, and high 12.2% (log rank P < 0.001); and OS: Low 64.4%, intermediate 58.3%, and high 13.6% (log rank P < 0.001) [Figure 2]b and [Figure 2]e. But this survival difference among LNRCs was seen only in LNT ≥10 group. In patients with LNT <10, the survival difference was not significant in various LNR categories: DFS (low 60%, intermediate 31.2%, high 54%; log rank P = 0.764) and OS (low 80%, intermediate 72.7%, high 58.2%; log rank P = 0.739).

Analysis of molecular subgroups across various LNRC in LNT ≥10 revealed that proportion of triple negative breast cancer (TNBC) decreased with increasing LNRC: low 52.1% (n = 41), intermediate 47.2% (n = 17) and high 26.5% (n = 9), compared with the 56.2% of the ypN0 (n = 41). On the other hand, proportion of luminal type (HR+) and Her2 enriched type of breast cancer increased with increasing LNRC: HR+ (20.8% low, 36.1% intermediate and 35.3% high versus 19.2% ypN0 cohort), Her2+ (27.1% low, 16.7% intermediate, and 38.2% high versus 9.6% ypN0 cohort) [Table 3].

Survival analysis across various molecular subtypes by LNRC revealed an inverse relationship between LNRC and DFS in TNBC (68.7% low, 56% intermediate, and 0 high; log rank P < 0.001) and Her2 enriched breast cancer (66.7% low, 33.3% intermediate and 40.9% high; log rank P = 0.045), but not in luminal types (46.9% low, 64.3% intermediate, 30.9% high; log rank P = 0.073) [Table 4]. The same inverse association was observed between OS and LNRC across various molecular subtypes [Table 4]. In decreasing order of significance, the 5 year OS in triple negative breast cancer was most significantly associated with increasing LNRC (78.5% low, 51.9% intermediate, and 0 high; log rank P < 0.001) followed in order by Her2 enriched (80% low, 44.4% intermediate, and 23.1% high); log rank P = 0.005) and luminal type (75% low, 72.7% intermediate, and 51.9% high; log rank P = 0.024) [Figure 3]a, [Figure 3]c and [Figure 3]e.
Table 4: 5-year Disease-free survival (DFS) and Overall survival (OS) by IHC subtypes

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Figure 3: 5-year overall survival in various breast cancer intrinsic subtypes by lymph node ratio category (LNRC) and single cut-off value 0.25. (a) Luminal and LNRC; (b) Luminal and single LNR value; (c) HER2 enriched and LNRC; (d) HER2 enriched and single LNR value; (e) TNBC and LNRC; (f) TNBC and single LNR value

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Pre-treatment clinical nodal staging was available in 97.8% (n = 219). A total of 66 (31%) of the 213 clinically node positive patients were downstaged from clinically node positive to pathologically node negative. In contrast, 48/213 (22.5%) patients were upstaged: 17 (8%) luminal type, 13 (7%) Her2+ enriched type and 45 (21.1%) triple negative type. Out of 6 clinically node negative patients, 2 (33.3%) patients were upstaged and both of them had Her2 enriched type of breast cancer. In the cases which were upstaged, median LNR was 0.75 (0.3-1) in luminal type, 0.8 (0.3-1) in Her2+ enriched type, and 0.45 (0.2-0.9) in triple negative breast cancer. Also, 71/213 (33.3%) patients had no change in nodal stage following NACT.

We also tried to explore a single LNR value which could discriminate between favourable and unfavourable DFS and OS. The cut-off value of 0.25 was found to be significantly associated with survival. 5 year DFS analysed by a LNR value ≤0.25 versus LNR value >0.25 was 62.7% versus 43.2%, log rank P = 0.002 and 5-year OS was 96.8% versus 82.6%, log rank P = 0.024 [Figure 2]c and [Figure 2]f. Analysis across molecular subtypes revealed that LNR value ≤0.25 was significantly associated with DFS in TNBC cases, 71.4% versus 27.8%; log rank P = 0.001 and Her2+ positive tumours 61.3% versus 33.6%; log rank P = 0.013. However, this cut off value was not significant for HR+ tumors (59.6% versus 27.9%; log rank P = 0.132). On the other hand, the LNR value ≤0.25 was significantly associated with OS across all molecular subtypes in decreasing order of significance across TNBC (77.3% versus 34.8%; log rank P < 0.001), Her2+ tumors (78.4% versus 32.0%; log rank P = 0.001), and HR+ tumors (67.7% versus 39.6%; log rank P = 0.144) [Figure 3]b, [Figure 3]d and [Figure 3]f.

 » Discussion Top

The results of this study show that: (1) LNR was an independent prognostic parameter along with the AJCC ypN stage in node positive patients, in whom ≥ 10 LNs have been removed; (2) Previously validated LNR categories were found to significantly distinguish between favourable and unfavourable outcomes in all molecular subtypes of breast cancer; (3) The single cut-off LNR value of 0.25 was found to be significantly associated with survival in TNBC and HER2-positive tumors.

Residual disease after NAC, especially in lymph nodes, is associated with poor prognosis.[13],[14],[15] This is very much reflected in the current study as well where ypN+ patients had a significantly poorer survival than ypN0 patients [Figure 2]a and [Figure 2]d. Adequate lymph node dissection (dissection of at least 10 axillary LN) is important for proper staging of axilla.[2],[16],[17] The differences in the number of LNs retrieved may be explained on the basis of variability of intrinsic anatomy, surgical expertise, institutional protocol, and the pathologists' experience and probably the type of chemotherapy.[18] Nodal involvement is less common in TNBC, compared to HER2-positive and Hormone receptor (HR) positive subtypes. On the contrary, TNBC and HER2-positive tumors are more likely to achieve a pCR as compared to HR-positive tumors. These differences in pCR rate in response to NAC across TNBC and HR-positive subtypes are reflected in our study. We did not find the same response in HER2-positive patients, possibly because of non-usage of anti-Herceptin therapy in this subset of patients [Table 2].

The association between LNRC and survival has been investigated in the adjuvant and neoadjuvant setting in various studies.[9],[11],[19],[20] In the neoadjuvant setting, LNR has been demonstrated to have some prognostic significance with conflicting results.[19],[20] Wu et al. showed that LNR is an independent predictor of DFS and OS irrespective of the number of lymph nodes removed.[21] On the contrary, Wapnir et al. demonstrated the significant association between LNR and DFS only in TNBC and HR-positive patients with ≥10 lymph nodes dissected out.[20] In our study, we found significant association between LNR and DFS only in TNBC and HER2-positive tumors. We also found an association between LNR and OS across all molecular subtypes (in decreasing order of significance; TNBC > HER2-positive > HR-positive tumors). However, this association was seen only in adequately sampled axilla (≥10 LN removed) [Table 4] and [Figure 3]a, [Figure 3]b, [Figure 3]c.

Keam et al. have suggested the use of 0.25 as a single cut-off value, while Wapnir et al. found the cut off value 0.15 as prognostic in HR-positive and TNBC cancers.[19],[20] In the present series, LNR ≤0.25 was found to discriminate between favourable and unfavourable outcome in TNBC and HER2-positive breast cancer, but not in HR-positive breast cancer [Figure 3]b, [Figure 3]d and [Figure 3]f.

We acknowledge that our study suffers from several shortcomings, including a retrospective study design; adjuvant treatment taken after surgery is not taken into account; clinical T and N stage were based on clinical examination only and not imaging; molecular subtypes were defined based only on ER, PR and Her2 status because of the non-availability of Ki67 and grade (in 46.7% patients); and neoadjuvant anti HER2 treatment was not given in Her2 enriched subtype because of the non-availability and also the non-affordability of the treatment by many patients. However, the current study has the strength of long follow-up with only 4% of patients being lost to follow up over the 11 years' study period.

 » Conclusion Top

In conclusion, the current study demonstrates that with the integrated use of the LNR and ypN in locally advanced breast cancer patients in various molecular subtypes, both the LNR category and the single cut-off value help in predicting the prognosis, and it may help in tailoring adjuvant therapy. The LNR was found to impact survival in cases where the axilla was adequately sampled.

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Conflicts of interest

There are no conflicts of interest.

 » References Top

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Axelsson CK, Mouridsen HT, Zedeler K. Axillary dissection of level I and II lymph nodes is important in breast cancer classification. The Danish breast cancer cooperative group (DBCG). Eur J Cancer 1992; 28A: 1415-8.  Back to cited text no. 2
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Sosa JA, Diener-West M, Gusev Y, Choti MA, Lange JR, Dooley WC, et al. Association between extent of axillary lymph node dissection and survival in patient with stage I breast cancer. Ann Surg Oncol 1998; 5:140-9.  Back to cited text no. 4
van der Wal BC, Butzelaar RM, van der Meij S, Boermeester MA. Axillary lymph node ratio and total number of removed lymph nodes: Predictors of survival in stage I and II breast cancer. Eur J Surg Oncol 2002; 28:481-9.  Back to cited text no. 5
Fisher B, Brown A, Mamounas E, Wieand S, Robidoux A, Margolese RG, et al. Effect of preoperative chemotherapy on loco-regional disease in women with operable breast cancer: Findings from National surgical adjuvant breast and bowel project B-18. J Clin Oncol 1997; 15:2483-93.  Back to cited text no. 6
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Belanger J, Soucy G, Sideris L, Leblanc G, Drolet P, Mitchell A, et al. Neoadjuvant chemotherapy in invasive breast cancer results in a lower axillary lymph node count. J Am Coll Surg 2008; 206:704-8.  Back to cited text no. 8
Schiffman SC, McMasters KM, Scoggins CR, Martin RC, Chagpar AB. Lymph node ratio: A proposed refinement of current axillary staging in breast cancer patients. J Am Coll Surg 2011; 213:45-52.  Back to cited text no. 9
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Vinh-Hung V, Verooijen HM, Fioretta G, Neyroud-Caspar I, Rapiti E, Vlastos G, et al. Lymph node ratio as an alternative to pN staging in node positive breast cancer. J Clin Oncol 2009; 27:1062-8.  Back to cited text no. 11
Truong PT, Vinh-Hung V, Cserni G, Woodward WA, Tai P, Vlastos G. The number of positive nodes and the ratio of positive nodes to excised nodes are significant predictors of survival in women with micrometastatic node-positive breast cancer. Eur J Cancer 2008; 44:1670-7.  Back to cited text no. 12
Von Minckwitz G, Untch M, Blohmer JW, Costa SD, Eidtmann H, Fasching PA, et al. Definition and impact of pathologic complete response on prognosis after neoadjuvant chemotherapy in various intrinsic breast cancer subtypes. J Clin Oncol 2012; 30:1796-804.  Back to cited text no. 13
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Choi M, Park YH, Ahn JS, Im YH, Nam SJ, Cho SY, et al. Evaluation of pathologic complete response in breast cancer patients treated with neoadjuvant chemotherapy: Experience in a single institution over a 10-year period. J Pathol Trans Med 2017; 51:69-78.  Back to cited text no. 15
Mathiesen O, Carl J, Bonderup O, Panduro J. Axillary sampling and the risk of erroneous staging of breast cancer. An analysis of 960 consecutive patients. Acta Oncol 1990; 29:721-5.  Back to cited text no. 16
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Schaapveld M, Otter R, de Vries EG, Fidler V, Grond JAK, van der Graff WTA, et al. Variability in axillary lymph node dissection for breast cancer. J Surg Oncol 2004; 87:4-12.  Back to cited text no. 18
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  [Figure 1], [Figure 2], [Figure 3]

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

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