Omission of Axillary Lymph Node Dissection for Breast Cancer Patients with Three or More Positive Sentinel Lymph Nodes

doi:10.21203/rs.3.rs-2747638/v1

Purpose

The ACOSOG Z0011 (Z11) trial assessed the benefit of axillary dissection (ALND) for breast cancer patients with sentinel lymph node (SLN) metastases; however, Z11 excluded patients with ≥ 3 positive SLNs. We analyzed trends in ALND omission in patients with ≥ 3 positive SLNs.

Methods

Women with ≥ 3 positive SLNs who underwent breast-conserving surgery (BCS) or mastectomy between 2018–2020 in the National Cancer Database were included using SLN codes initiated in 2018. Patients with stage IV disease, recurrent breast cancer, and who underwent neoadjuvant chemotherapy were excluded. A multivariable logistic regression model was utilized to determine the proportion who received ALND and factors associated with ALND omission. A subgroup analysis was performed among patients who met the remainder of the Z11 inclusion criteria (BCS, T1/T2 breast cancer).

Results

We identified 3654 patients with ≥ 3 positive SLNs. ALND was omitted in 37% of patients, and omission significantly increased from 2018 to 2020 (29% vs 41%, p < 0.0001). Older age, lower grade tumors, no radiation, non-academic facility, BCS, more SLNs examined and fewer positive SLNs were significantly associated with ALND omission. 942 patients with ≥ 3 positive SLNs met the remainder of the Z11 inclusion criteria. ALND was omitted in 49% of these patients, and omission increased from 2018 to 2020 (44% vs 49%, p = 0.22).

Conclusion

Approximately one-third of patients with ≥ 3 positive SLNs do not undergo ALND; omission of ALND increased from 2018 to 2020. Studies assessing oncologic outcomes of patients with ≥ 3 positive SLNs who do and do not receive ALND are required.

sentinel lymph node

axillary lymph node dissection

Z0011 trial

trends in omission

The practice changing ACOSOG Alliance Z0011 (Z11) randomized clinical trial found no difference in survival between axillary observation versus axillary lymph node dissection (ALND) for women who underwent breast-conserving surgery (BCS) and tangential whole-breast radiation with 1 or 2 positive sentinel lymph nodes (SLNs) [1]. Consequently, the use of ALND for lymph node-positive breast cancer has substantially declined [2–5]. However, questions remain regarding axillary management of patients with ≥ 3 positive SLNs as they were excluded from the Z11 study.

Beginning in 2018, the National Cancer Database (NCBD) required Commission on Cancer-accredited facilities to include the exact number of positive SLNs to reduce unrecorded SLN biopsies (SLNB) and to distinguish positive SLN from those identified during ALND [6]. The objective of our study was to assess the current trends of ALND omission in women with breast cancer and ≥ 3 positive SLNs using novel NCDB codes. Additionally, we aimed to assess adherence to the Z11 recommendations of performing ALNDs in the subset of patients with T1/T2 breast cancer and ≥ 3 positive SLNs who had undergone breast-conservative surgery (BCS).

The NCDB is a joint project of the Commission on Cancer (CoC) of the American College of Surgeons and the American Cancer Society. The data used in the study are derived from a de-identified NCDB file. The American College of Surgeons and the Commission on Cancer have not verified and are not responsible for the analytic or statistical methodology employed, or the conclusions drawn from these data by the investigator [7]. The NCDB is a nationwide hospital-based dataset that collects comprehensive patient, disease and treatment characteristics and reports on 70% of the new cancer cases in the United States [8, 9]. The University of Minnesota Institutional Review Board (IRB) deemed this study exempt from the IRB’s review and patients’ informed consent secondary to its use of de-identified data.

Patients with T1-T3 breast cancer and ≥ 3 positive SLNs who underwent mastectomy or BCS between 2018–2020 were identified from the NCDB, using the novel SLN codes introduced in 2018. Patients who received neoadjuvant chemotherapy, had stage IV disease, had T4 disease, underwent a radical mastectomy, and had recurrent breast cancer were excluded. We determined how many patients received ALND and used a multivariable logistic regression model to identify factors associated with omission of ALND. Age, race, academic facility, Charlson comorbidity index (CCI), hormone receptor status, grade, tumor size, radiation status, type of surgery, the specific number of positive SLNs and the total number of SLNs removed were analyzed. A subgroup analysis was performed on patients who otherwise fulfilled Z11 inclusion criteria (BCS, T1/T2 breast cancer) but had ≥ 3 positive SLN.

We identified 3654 patients with T1-T3 breast cancer and ≥ 3 positive SLNs who underwent mastectomy or BCS between 2018–2020. Most patients were ≥ 65 years, non-Hispanic White, treated at a non-academic facility, had a CCI score of 0, underwent a total mastectomy, and received radiation (Table 1). Most tumors were hormone receptor positive, 2-5cm in size and grade 1 or 2. Overall, 37% of patients with ≥ 3 positive SLN did not undergo ALND. On univariate analysis, older age, non-academic facility, progesterone receptor positivity, lower grade tumors, tumors ≤ 5cm, BCS, and lack of radiation were significantly associated with ALND omission (Table 2). A higher number of SLNs examined was significantly associated with omission of ALND; the number of positive SLNs was not significantly associated with omission of ALND (Table 2). On multivariable analysis, older age, lower grade tumors, BCS, lack of radiation, non-academic facility, higher number of SLNs examined and lower number of positive SLNs were significantly associated with omission of ALND (Table 3). ALND omission increased significantly from 2018 to 2020 (29% vs 41%, p < 0.0001) (Fig. 1).

Table 1

Cohort characteristics of patients with ≥ 3 positive sentinel lymph nodes (SLN) from the National Cancer Database (2018–2020)
	≥ 3 positive SLNs (n = 3654)
	n	%
Age at Diagnosis (years)
18–44	828	23
45–54	915	25
55–64	861	24
65+	1050	29
Race
Non-Hispanic White	2467	68
Black	521	14
Other	666	18
Charlson Comorbidity Index
0	3035	83
1	433	12
2	114	3
3	72	2
Academic Center
No	2629	72
Yes	1025	28
Estrogen Receptor Status
Positive	3068	84
Negative	586	16
Progesterone Receptor Status
Positive	2755	75
Negative	899	25
Grade
1 and 2	2072	57
3	1155	32
Missing	427	12
Tumor Size
< 2 cm	954	26
2–5 cm	1884	52
> 5 cm	715	20
Missing	101	3
Radiation
Yes	2901	79
No	681	19
Missing	72	2
Surgery Type
Breast-Conserving Surgery	1305	36
Mastectomy	2349	64
Axillary Surgery Type
SLNB alone	1345	37
ALND +/- SLNB	2309	63
Number of SLNs Examined
3	657	18
4	684	19
5	532	15
6+	1781	49
Number of positive SLNs
3	2019	55
4	751	21
5	350	10
6+	534	15

Table 2

Univariate analysis of factors associated with omission of axillary lymph node dissection (ALND) in patients with ≥ 3 positive sentinel lymph nodes (SLN) from the National Cancer Database (2018–2020)
	SLN only (n = 1345)		ALND (n = 2309)		p-value
	n	%	n	%
Age at Diagnosis (years)
18–44	252	19	576	25	< 0.0001
45–54	301	22	614	27
55–64	303	23	558	24
65+	489	36	561	24
Race
Non-Hispanic White	921	68	1546	67	0.62
Black	188	14	333	14
Other	236	18	430	19
Charlson Comorbidity Index
0	1104	82	1931	84	0.11
1	157	12	276	12
2	52	4	62	3
3	32	2	40	2
Academic Center
No	1006	75	1623	70	0.004
Yes	339	25	686	30	0.004
Estrogen Receptor Status
Positive	1144	85	1924	83	0.17
Negative	201	15	385	17	0.17
Progesterone Receptor Status
Positive	1041	77	1714	74	0.03
Negative	304	23	595	26	0.03
Grade
1 and 2	808	60	1264	55	0.0008
3	374	28	781	34
Missing	163	12	264	11
Tumor Size
< 2 cm	375	28	579	25	0.004
2–5 cm	720	54	1164	50
> 5 cm	216	16	499	22
Missing	34	3	67	3
Radiation
Yes	1028	76	1873	81	0.003
No	284	21	397	17
Missing	33	2	39	2
Surgery Type
Breast Conserving Surgery	611	45	694	30	< 0.0001
Mastectomy	734	55	1615	70	< 0.0001
Number of SLNs Examined
3	189	14	468	20	< 0.0001
4	239	18	445	19
5	201	15	331	14
6+	716	53	1065	46
Number of positive SLNs
3	757	56	1262	55	0.64
4	272	20	479	21
5	119	9	231	10
6+	197	15	337	15

Table 3

Multivariable analysis of factors associated with omission of axillary lymph node dissection (ALND) within the overall cohort of patients with ≥ 3 positive sentinel lymph nodes (SLN) and the subset of patients that fulfill the remaining Z0011 trial criteria from the National Cancer Database (2018–2020)
	Overall Cohort: ≥ 3 positive SLN (n = 3654)		T1/2 tumors + ≥ 3 positive SLN + breast conserving surgery (n = 942)
	OR	95% CI	OR	95% CI
Age at Diagnosis (years)
18–44	REF		REF
45–54	1.13	0.97–1.33	1.41	1.01–1.98
55–64	1.10	0.94–1.29	1.28	0.92–1.77
65+	1.39	1.19–1.63	1.77	1.27–2.45
Race
Non-Hispanic White	REF		REF
Black	0.95	0.81–1.11	0.88	0.66–1.18
Other	1.01	0.88–1.16	0.80	0.61–1.05
Charlson Comorbidity Index
0	REF		REF
1	0.91	0.77–1.07	0.95	0.71–1.28
2	1.07	0.78–1.45	1.04	0.62–1.76
3	1.40	0.97–2.03	2.51	1.14–5.51
Academic Center
No	REF		REF
Yes	0.78	0.69–0.88	0.83	0.67–1.02
Estrogen Receptor Status
Positive	REF		REF
Negative	1.08	0.87–1.34	1.12	0.65–1.93
Progesterone Receptor Status
Positive	REF		REF
Negative	0.96	0.81–1.15	1.14	0.77–1.68
Grade
1 and 2	REF		REF
3	0.84	0.74–0.96	0.81	0.63–1.03
Missing	0.94	0.80–1.10	1.05	0.77–1.42
Tumor Size
< 2 cm	REF		REF
2–5 cm	1.01	0.89–1.13	1.09	0.89–1.32
> 5 cm	0.89	0.76–1.06	n/a	n/a
Missing	0.98	0.67–1.44	n/a	n/a
Radiation
Yes	REF		REF
No	1.32	1.14–1.52	1.51	1.10–2.08
Missing	1.72	1.16–2.56	1.36	0.63–2.95
Surgery Type
Breast Conserving Surgery	REF		n/a
Mastectomy	0.55	0.50–0.62	n/a
Number of SLNs Examined
3	0.44	0.37–0.52	0.49	0.37–0.66
4	0.66	0.56–0.76	0.88	0.67–1.15
5	0.85	0.72-1.00	1.01	0.76–1.35
6+	REF		REF
Number of positive SLNs
3	REF		REF
4	0.80	0.70–0.92	0.68	0.52–0.88
5	0.67	0.55–0.81	0.55	0.37–0.80
6+	0.67	0.56–0.79	0.58	0.39–0.86

We identified 942 patients who had ≥ 3 positive SLNs but met the remainder of the Z11 inclusion criteria. Within this subset, 49% did not undergo ALND. On univariate analysis, older age, higher CCI, lack of radiation, and larger number of SLNs examined were significantly associated with ALND omission (Table 4). On multivariable analysis, ages 45–54 years and ≥ 65 years, higher CCI, lack of radiation, higher number of SLN examined and fewer positive SLN were associated with ALND omission (Table 3). Within this subset of the population, ALND omission increased from 2018 to 2020 however this difference was not significant (44% vs 49%, p = 0.22) (Fig. 1).

Table 4

Univariate analysis of factors associated with omission of axillary lymph node dissection (ALND) in patients with ≥ 3 positive sentinel lymph nodes (SLN) and fulfill the remaining Z0011 trial criteria from the National Cancer Database (2018–2020)
	SLNB only (n = 461)		ALND (n = 481)		p-value
	n	%	n	%
Age at Diagnosis (years)
18–44	37	8	71	15	0.0003
45–54	94	20	102	21
55–64	124	27	148	31
65+	206	45	160	33
Race
Non-Hispanic White	337	73	325	68	0.06
Black	63	14	66	14
Other	61	13	90	19
Charlson Comorbidity Index
0	364	79	398	83	0.004
1	58	13	63	13
2	22	5	18	4
3	17	4	2	0
Academic Center
No	320	69	312	65	0.12
Yes	141	31	169	35	0.12
Estrogen Receptor Status
Positive	428	93	444	92	0.75
Negative	33	7	37	8	0.75
Progesterone Receptor Status
Positive	405	88	412	86	0.32
Negative	56	12	69	14	0.32
Grade
1 and 2	304	66	310	64	0.13
3	94	20	120	25
Missing	63	14	51	11
Tumor Size
< 2 cm	189	41	203	42	0.71
2–5 cm	272	59	278	58	0.71
Radiation
Yes	367	80	416	86	0.02
No	81	18	55	11
Missing	13	3	10	2
Surgery Type
Breast Conserving Surgery	466		481
Number of SLNs Examined
3	74	16	113	23	< 0.0001
4	108	23	89	19
5	78	17	73	15
6+	201	44	206	43
Number of positive SLNs
3	316	69	305	63	0.27
4	74	16	83	17
5	32	7	45	9
6+	39	8	48	10

Within our overall cohort, 37% of patients with ≥ 3 positive SLNs from breast cancer did not undergo ALND. Additionally, omission of ALND increased significantly from 2018–2020. We found that omission of ALND was independently and significantly associated with older age, lower grade tumors, BCS, lack of radiation, non-academic facility, higher number of SLNs examined and lower number of positive SLNs. Within our Z11 subgroup, ALND was omitted in 49% of patients with ≥ 3 positive SLN. Though not statistically significant, omission of ALND increased from 2018 to 2020.

The ACOSOG Z0011 phase 3 randomized clinical trial included women with clinically node-negative, T1/T2 breast cancer, and 1–2 positive SLNs who underwent BCS and whole breast radiation. Patients were randomized to axillary observation versus completion ALND [1]. The 10-year overall survival, loco-regional recurrence, and disease-free survival rates were not significantly different between ALND and observation [10, 11]. Based on these findings, breast cancer management guidelines were updated to avoid ALND for patients who fulfill Z11 inclusion criteria [12].

Other studies have also assessed the impact of ALND vs observation for patients with SLN metastases. Recently, the multicenter, randomized clinical trial SINODAR-ONE reported similar 3-year survival and relapse rates with ALND vs observation for patients with T1/2 breast cancers and 1–2 positive SLNs with macrometastases [13]. IBCSG 23 − 01 reported similar 5-year and 10- year disease-free survival rates with ALND vs observation for patients with T1/T2 tumors, no palpable axillary adenopathy and ≥ 1 positive SLN with micrometastasis (≤ 2mm) [14, 15]. The multicenter, randomized clinical trial AMAROS (EORTC 10981–22023 AMAROS) reported no significant differences in disease-free survival (DFS), overall survival and axillary recurrence rates with ALND vs axillary radiotherapy for patients with no palpable lymph nodes, T1/2 breast cancer, and ≥ 1 positive SLN with micro or macrometastasis [16]. The Z11 trial only included patients who underwent BCS, while these other clinical trials included a small proportion of patients who underwent mastectomy. The inclusion criteria of these trials likely influence the surgical management of SLN metastases in the United States, because we found that patients undergoing BCS were more likely to omit ALND.

SLN biopsy is currently recommended by the National Comprehensive Cancer Network(NCCN) guidelines for patients with no palpable lymph nodes and ≤ 2 nodes that are positive through needle biopsy or are suspicious on imaging [12]. NCCN guidelines recommends that if the SLN is positive and the patient undergoes BCS, then all the following criteria must be met to avoid an ALND: cT1/T2 disease, ≤ 2 positive SLNs, no neoadjuvant chemotherapy, and planned whole breast radiation therapy. If a mastectomy is completed, similar criteria must be met, however, axillary directed radiation therapy must be included [12].

The data regarding outcomes of patients with ≥ 3 positive SLNs are limited. In the AMAROS trial, only 5% had ≥ 3 positive SLNs [16]. In the IBCSG 23 − 01 randomized controlled trial, only 1 patient with 3 positive SLNs was included [14]. A meta-analysis compared ALND vs SLNB alone in patients with T1/T2 breast cancer and included patients with ≥ 3 positive SLNs. No difference in survival was reported, however, < 9% of patients had ≥ 3 positive SLNs within each group [17]. Bonneau et al published a retrospective cohort study using the Surveillance, Epidemiology, and End Results (SEER) database in 2015 assessing overall survival and specific survival of T1-T2 breast cancer patients with ≥ 3 positive lymph nodes who underwent SLNB alone vs ALND. Overall and cancer-specific survival were not different between the two groups and only 4% of patients received SLNB alone [18]. Additionally, this study was published prior to SEER releasing the variable “SLNs positive” in 2018.

Previous NCDB studies are limited due to the lack of codes tracking the type of axillary surgery and/or the number of positive SLNs [19, 20]. A retrospective cohort study by Yao et al utilized NCDB to assess patients who fulfilled the majority of Z11 criteria similar to our study (BCS, T1-T2, ≥ 3 positive lymph nodes). The authors found that SLNB alone increased significantly from 1998 to 2011, however SLNB and ALND were arbitrarily clarified as ≤ 4 nodes vs ≥ 10 nodes respectively [4]. Recently, Stafford et al utilized the new 2018 NCDB codes reporting positive SLNs to assess trends in axillary surgery, however the study limited the cohort to patients with 1–2 positive SLNs [21].

To our knowledge, this is the first study to use the NCDB to accurately assess the trends of axillary surgery in patients with ≥ 3 positive SLNs. Previous studies are limited in the availability of NCDB codes to accurately track the type of axillary surgery completed as well as the number of positive SLNs. Additionally, most of our cohort consists of patients who underwent mastectomies when literature has focused on BCS in the past.

We recognize several limitations of our study, including lack of survival data due to the recent time period of the study. Tumor registrar coding of American Joint Committee on Cancer (AJCC) staging in the NCDB also has the potential for error. Of note, a large percentage of the cohort was recorded to have ≥ 6 SLNs examined, despite specific coding instructions on identification and separation of examined SLNs versus overall regional lymph nodes removed. A histogram depicting the distribution of reported SLNs is included (Online Resource). This observation may be related to over-counting SLNs due to the technique of cutting SLNs. Weaver describes this problem when the initial pathologist/technician cuts the SLN, but the final pathologist counts each individual cut as a node [22]. Furthermore, NCDB does not record the extent of SLN involvement: the size of metastatic deposits or the presence of extranodal extension. As this is a retrospective study, selection bias regarding which patients undergo SLNB alone or ALND is present. Despite these limitations, this study includes a large number of patients with ≥ 3 positive SLNs and represents the current management in the United States.

Using the novel NCDB codes to accurately track positive SLNs, we found that approximately one-third of patients with ≥ 3 positive SLNs do not undergo ALND, and omission of ALND increased during our study period. Though omission of ALND avoids a morbid operation for women, the potential oncologic benefits for ALND are unknown for this group of patients. Future research should include studies that focus on understanding the impact of axillary surgery on oncologic outcomes of patients with ≥ 3 positive SLNs. Such research will further inform the oncologic safety of de-escalation of axillary surgery.

Declarations of interest: none.

Funding: The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Competing Interest: The authors have no relevant financial or non-financial interests to disclose.

Author contributions: All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Schelomo Marmor. The first draft of the manuscript was written by Saranya Prathibha and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Data Availability: The datasets generated during and/or analyzed during the current study are not publicly available due to the National Cancer Database’s data use agreement. Only hospitals that provide data to the NCDB are allowed to access the dataset, but the dataset are available from the corresponding author on reasonable request.

Ethics Approval and Consent to Participate and Publish: The University of Minnesota Institutional Review Board (IRB) deemed this study exempt from the IRB’s review and patients’ informed consent to participate and publish secondary to its use of de-identified data.

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Omission of Axillary Lymph Node Dissection for Breast Cancer Patients with Three or More Positive Sentinel Lymph Nodes

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