Effect of postmastectomy radiotherapy on T1-2N1M0 triple-negative breast cancer

doi:10.21203/rs.3.rs-379848/v1

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Effect of postmastectomy radiotherapy on T1-2N1M0 triple-negative breast cancer

https://doi.org/10.21203/rs.3.rs-379848/v1

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Background: The effect of postmastectomy radiotherapy (PMRT) on T1-2N1M0 triple-negative breast cancers (TNBC) remains unclear. The population-based study aimed to investigate the survival outcomes of T1-2N1M0 TNBC patients who underwent PMRT or not.

Methods: We selected 1743 patients with T1-2N1M0 TNBC who underwent mastectomy between 2010 and 2015 through the Surveillance, Epidemiology and End Results (SEER) database. After propensity score matching (PSM) , the PMRT and no-PMRT groups consisted of 586 matched patients, respectively.The Kaplan-Meier method was applied to calculate breast cancer-specific survival (BCSS) and cox proportional hazard model were used to determine the prognostic factors of T1-2N1M0 TNBC.

Results: The 5-year BCSS for the PMRT group and no-PMRT group was 79.1% and 74.7%, respectively. TNBC patients with stage T1-2N1M0 receiving PMRT did not show better BCSS than those did not (HR =0.800, 95% CI =0.605-1.056, P =0.115). Subgroup analysis showed that in patients with three nodes positive, radiotherapy could significantly improve BCSS(HR=0.396, 95% CI = 0.175-0.900, P = 0.027), but it brought no significant advantage in BCSS in patients with one or two nodes positive(HR =1.061, 95% CI =0.725-1.552, P =0.761; HR =0.657, 95% CI =0.405-1.065, P =0.088).In addition, PMRT improves the BCSS in TNBC patients with T2 tumor concomitant with three positive lymph nodes(HR =0.343, 95% CI =0.132-0.890, P =0.028).

Conclusion: TNBC patients with T2 tumor concomitant with three positive lymph node can benefit from PMRT.

Oncology

triple-negative breast cancer

postmastectomy

radiotherapy

prognosis

TNBC is defined as breast cancer that lacks estrogen receptor, progesterone receptor expression and human epidermal growth factor receptor 2 (HER-2) over-expression or gene amplification, accounting for 10% ~ 15% of all breast cancer [1-3].As a special type of breast cancer, TNBC has a special biological behavior, with a high degree of malignancy and early recurrence and metastasis [4-6].

Due to the lack of therapeutic targets, TNBC does not benefit from endocrine therapy and anti-HER-2 targeted therapy.At present, the main clinical treatment is surgery combined with radiotherapy and chemotherapy. Chemotherapy is one of the main means of systemic treatment for TNBC patients, while surgery and radiotherapy are the main local treatment for TNBC patients.Currently, the indications for adjuvant radiotherapy after mastectomy are primary tumor diameter≥ 5cm or the number of axillary lymph node metastases ≥ 4, while there is still controversy about whether adjuvant radiotherapy is necessary for T1-2 breast cancer patients with 1 to 3 axillary lymph node metastasis [7,8].Studies have found no significant improvement in DFS and OS in T1-2N1M0 TNBC patients receiving PMRT [9,10]. On the contrary, other studies have confirmed that T1-2N1M0 TNBC patients can benefit from PMRT [11,12].In the available evidence, the effect of PMRT on T1-2N1M0 TNBC patients is contradictory, and the value of PMRT on T1-2N1M0 TNBC patients needs to be further clarified.In this study, we investigated the effect of PMRT on BCSS In T1-2N1M0 TNBC patients, and performed subgroup analyses to determine which patients could benefit from PMRT.

Patients

We collected data from the SEER database for this study. The inclusion criteria included: (1) female; (2) 20-79 years old; (3) diagnosed with TNBC from 2010 to 2015; (4) T1-2N1M0; (5) The mastectomy was performed. Exclusion criteria included:(1) patients who did not undergo axillary dissection; (2) patients with unknown clinicopathologic characteristics; (3) patients without radiotherapy record or chemotherapy record.

We collected the following variables: age, year of diagnosis, race, marital status, histology, histological grade, number of lymph nodes (LNs) positive, chemotherapy record, radiotherapy record, follow-up time, vital status.

Statistical analysis

The main outcome of interest was BCSS, which was calculated from the date of diagnosis to the date of death due to breast cancer.The clinicopathologic characteristics of the PMRT and no-PMRT groups were compared through the X² test.One-to-one (1:1) PSM was used to create a matched dataset to balance the baseline characteristics between the two groups.The survival curve of BCSS was plotted by the Kaplan-Meier product limit method and compared by the log rank test. A Cox proportional hazards regression model was used to analyze the prognostic factors associated with BCSS.P values were two-sided, and P<0.05 was considered statistically significant. These analyses were performed using the SPSS version 20.0 software package (IBM SPSS Statistics, Chicago, IL, US) and the R Project (R version 3.6.2 for Windows).

Patient characteristics

1743 patients diagnosed with T1-2N1M0 TNBC from 2010 to 2015 were recruited to the study. They were divided into the PMRT(789, 45.27%) and no-PMRT (954, 54.73%) groups. Compared with the no-PMRT group, patients in the PMRT group were older, had higher grades, had larger tumors, had more positive lymph nodes, were more likely to receive chemotherapy, and had a higher proportion of invasive ductal carcinoma(P<0.05).After PSM, the PMRT and no-PMRT groups consisted of 586 matched patients, respectively.There were no significant differences between the variables of the two groups after PSM(P>0.05).Table 1 summarizes the patient characteristics of the two groups.

Prognostic factors associated with BCSS

We compared the BCSS of the PMRT and no-PMRT groups.With a median follow-up of 49.5 months, the 5-year BCSS for the PMRT group and no-PMRT group was 79.1% and 74.7%, respectively(Log-rank P=0.166, Figure 1A). We studied the prognostic factors associated with BCSS.Univariate analysis indicated that BCSS was related to marital status, tumor size, number of positive LNs (all P<0.05), multivariate analysis showed that tumor size(P=0.007) and two positive LNs (P=0.005) were associated with BCSS.However, chemotherapy and radiotherapy had no statistically significant impact on the BCSS of T1-2N1M0 TNBC (all P>0.05)(Table 2).

Subgroup analyses of BCSS

We conducted subgroup analyses to determine the effect of radiotherapy on BCSS for T1-2N1M0 TNBC patients in different features (Table 3). Univariate analysis indicated that PMRT could improve the BCSS in patients with three nodes positive(HR =0.423, 95% CI = 0.190-0.941, P = 0.035), but it brought no significant advantage in BCSS in other patients. Multivariate analysis also showed that PMRT could improve the BCSS in patients with three nodes positive (HR =0.396, 95% CI = 0.175-0.900, P = 0.027; Figure 1D), but could not improve BCSS in patients with one or two nodes positive(HR =1.061, 95% CI =0.725-1.552, P =0.761; HR =0.657, 95% CI = 0.405-1.065, P = 0.088) (Figure 1B; Figure 1C).

Furthermore, To investigate the effect of PMRT on BCSS for TNBC patients with a certain tumor size and number of positive LNs, we crossed tumor size with number of positive LNs to divide patients into six subgroups( Figure 2). Multivariate analysis indicated that PMRT could improve the BCSS in TNBC patients with T2 tumor concomitant with three positive LNs (HR =0.343, 95% CI = 0.132-0.890, P = 0.028). However, other subgroups could not benefit from PMRT(Figure 3).

We used SEER database to study the influence of PMRT on BCSS in T1-2N1M0 TNBC patients, and conducted subgroup analysis to find out the subgroups that could really benefit from PMRT. The study showed that T1-2N1M0 TNBC patients with three nodes positive could get BCSS improvement from radiotherapy, in which the patients with T2 tumor concomitant with three positive LNs benefit significantly.Our study provided evidence for the management of PMRT for T1-2N1M0 TNBC patients.

Currently, the management of PMRT in T1-2N1M0 breast cancer patients remains controversial. Some studies have confirmed that such patients can benefit from PMRT [13-15], while some studies have drawn the opposite conclusion [16-17].In view of the high invasiveness and early recurrence of TNBC, local radiotherapy is particularly important.A study explored the effect of PMRT on T1-2N1M0 patients according to molecular typing, and the results showed that PMRT can reduce the local recurrence rate of TNBC patients [18].Gabos et al. also confirmed that PMRT can reduce the local recurrence rate, especially for women with T1-2N0 TNBC subtype [19].However, as with other subtypes of breast cancer, current recommendations for PMRT in T1-2N1M0 TNBC patients are controversial.

Tumor size and number of axillary lymph node metastases have been proved to be closely related to recurrence and prognosis of breast cancer [20,21].In our study, tumor size and number of positive LNs were associated with BCSS.The effect of PMRT mainly depends on the comprehensive consideration of tumor size and the number of positive LNs [22], and secondly, it is related to other high-risk factors such as young age and positive vascular tumor thrombus.Accordingly, we not only divided the subgroup analysis according to the clinicopathological characteristics, but also performed subgroup analysis by crossed tumor size with number of positive LNs, which proved that only BCSS in T2 patients with three positive LNs could benefit from PMRT.Zhang et al. studied the effect of PMRT on the survival of T1-4N1-N3M0 patients, and the results showed that there was no difference in BCSS between PMRT and non-PMRT cohort in the T1-2N1 subgroup (P = 0.191) [23], which was consistent with our results, but they did not conduct further stratified analysis.Another study included 675 T1-2N1M0 TNBC patients and subgroup analysis was performed based on the number of positive lymph nodes. After a median follow-up of 37 months, PMRT was independently associated with increased OS, but there was no improvement in BCSS in any subgroup[24].The reason why they are inconsistent with our conclusion may be due to their shorter follow-up time and fewer cases.

Radiotherapy can not only eliminate the residual lesions and reduce the recurrence rate of the disease, but also bring a series of complications, such as arm edema, cardiopulmonary radiation damage, pneumonia and so on [25-27].We need to comprehensively consider the benefits and side effects of radiotherapy for patients, identify the subgroups that can really benefit from radiotherapy, and optimize personalized treatment strategies.Our study conducted subgroup analyses based on clinicopathological characteristics and proves that radiotherapy did not provide survival benefit for T1-2 TNBC patients with 1 or 2 positive LNs. Chen et al. also showed that T1-2 breast cancer patients with one or two positive LNs could not benefit from PMRT [28].It may be that the tumor load and recurrence risk of these patients are low, radiotherapy has limited significance to improve their survival, and will instead bring side effects such as arm edema and cardiopulmonary radiation damage.For these patients, we should carefully choose radiotherapy to avoid overtreatment.

Our study has some limitations. First, we did not study the recurrence rate of patients due to that SEER database lacks recurrence data.Second, HER-2 status in SEER database was only available since 2010, so our follow-up period was relatively short. Third, SEER database does not provide detailed chemo-radiotherapy protocols.

In a word, our findings suggested that PMRT could significantly improve BCSS in T1-2N1M0 TNBC patients with three nodes positive, but it brought no significant advantage in BCSS in patients with one or two nodes positive. Patients with T2 tumor concomitant with three positive LNs benefit significantly from radiotherapy and should be advised to receive radiotherapy. Patients with one positive lymph node should not receive radiotherapy. For other patients, radiotherapy should be chosen carefully in combination with other high-risk factors.

- Ethics approval and consent to participate

Not applicable.

- Consent to publish

Not applicable.

- Availability of data and materials

Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov)

SEER*Stat Database: Incidence ‐ SEER 18 Regs Custom Data (with additional treatment fields), Available at: https://seer. cancer.gov/data/.

- Conflict of Interest

The author(s) declare that they have no competing interests.The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

- Funding

Not applicable.

- Authors' Contributions

Protocol/project development: L.-Y.X and W.-Y.X. Data acquisition and interpretation of data:L.-Y.X. Statistics analysis of data: L.-Y.X ,W.-Y.X and Y.Z. Manuscript drafting: L.-Y.X and Y.Z. Manuscript Revision and accountable for all aspects of the study:L.-Y.X, W.-Y.X and Y.Z. All authors read and approved the final manuscript.

- Acknowledgments

Not applicable.

TNBC = triple-negative breast cancer

PMRT= postmastectomy radiotherapy

PSM = propensity score matching

BCSS = breast cancer-specific survival

HER-2=human epidermal growth factor receptor 2

LN= lymph node

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Table 1 Baseline characteristics of the study population and tumor

Characteristics		before PSM			after PSM
Characteristics		PMRT (n,%)	No-PMRT (n,%)	P	PMRT (n,%)	No-PMRT (n,%)	P
No. of patients		789	954		586	586
Age (years)	20-49	375(47.53)	324(33.96)	<0.001	242(41.30)	243(41.47)	0.953
	50-80	414(52.47)	630(66.04)		344(58.70)	343(58.53)
Race	White	547(69.33)	713(74.74)	0.042	450(76.79)	444(75.77)	0.588
	Black	162(20.53)	159(16.67)		99(16.89)	96(16.38)
	Other	80(10.14)	82(8.59)		37(6.32)	46(7.85)
Marital status	Married	477(60.46)	583(61.11)	0.78	366(62.46)	362(61.77)	0.810
	Not married	312(39.54)	371(38.89)		220(37.54)	224(38.23)
Histology	IDC	72(91.25)	834(87.42)	0.010	535(91.30)	533(90.96)	0.837
	others	69(8.75)	120(12.58)		51(8.70)	53(9.04)
Grade	I+II	96(12.17)	165(17.30)	0.001	70(11.95)	67(11.43)	0.785
	III+IV	693(87.83)	739(82.70)		516(88.05)	519(88.57)
Tumor stage	T1	227(28.77)	363(38.05)	<0.001	174(29.69)	172(29.35)	0.898
	T2	562(71.23)	591(61.95)		412(70.31)	414(70.65)
No. of LNs positive	1	434(55.01)	625(65.51)	<0.001	362(61.77)	376(64.16)	0.693
	2	209(26.49)	248(26.00)		157(26.79)	146(24.91)
	3	146(18.50)	81(8.49)		67(11.43)	64(10.93)
Chemotherapy	yes	767(97.21)	776(81.34)	<0.001	565(96.42)	566(96.59)	0.874
	no	22(2.79)	178(18.66)		21(3.58)	20(3.41)

PSM= propensity score matching; PMRT= postmastectomy radiotherapy; LN= lymph node

Table 2 Prognostic factors for BCSS in univariate and multivariate analysis

Characteristics		Univariate		Multivariate
Characteristics		HR(95%CI)	P	HR(95%CI)	P
Age (years)	20-49	Ref.	Ref.	Ref.	Ref.
	50-80	1.241(0.933-1.650)	0.138	1.244(0.933-1.660)	0.137
Race	White	Ref.	Ref.	Ref.	Ref.
	Black	1.013(0.699-1.467)	0.947	0.932(0.639-1.358)	0.713
	Other	0.708(0.374-1.341)	0.289	0.686(0.361-1.305)	0.251
Marital status	Not Married	Ref.	Ref.	Ref.	Ref.
	Married	0.739(0.560-0.975)	0.033	0.766(0.575-1.019)	0.067
Histology	IDC	Ref.	Ref.	Ref.	Ref.
	others	0.560(0.305-1.028)	0.061	0.583(0.316-1.075)	0.084
Grade	I+II	Ref.	Ref.	Ref.	Ref.
	III+IV	1.145(0.722-1.817)	0.564	1.119(0.701-1.784)	0.638
Tumor stage	T1	Ref.	Ref.	Ref.	Ref.
	T2	1.631(1.168-2.277)	0.004	1.589(1.135-2.224)	0.007
No. of LNs positive	1	Ref.	Ref.	Ref.	Ref.
	2	1.590(1.175-2.152)	0.003	1.543(1.138-2.093)	0.005
	3	1.401(0.919-2.138)	0.117	1.275(0.833-1.953)	0.263
Chemotherapy	no	Ref.	Ref.	Ref.	Ref.
	yes	1.350(0.599-3.041)	0.469	1.344(0.592-3.050)	0.480
Radiotherapy	no	Ref.	Ref.	Ref.	Ref.
	yes	0.823(0.624-1.086)	0.168	0.800(0.605-1.056)	0.115

LN= lymph node

Table 3 Subgroup analysis of BCSS in univariate and multivariate analysis

Characteristics		Univariate		Multivariate
Characteristics		HR(95%CI)	P	HR(95%CI)	P
Age (years)	20-49	1.010(0.642-1.589)	0.996	0.960(0.609-1.514)	0.861
	50-80	0.724(0.510-1.029)	0.071	0.725(0.509-1.031)	0.074
Race	White	0.776(0.567-1.062)	0.113	0.746(0.544-1.022)	0.068
	Black	1.152(0.587-2.260)	0.680	1.142(0.581-2.246)	0.700
	Other	0.604(0.154-2.363)	0.469	0.844(0.186-3.833)	0.826
Marital status	Not Married	0.825(0.542-1.257)	0.371	0.835(0.547-1.275)	0.404
	Married	0.822(0.569-1.188)	0.297	0.781(0.539-1.131)	0.191
Histology	IDC	0.814(0.612-1.083)	0.157	0.793(0.596-1.056)	0.112
	others	0.954(0.289-3.147)	0.938	0.963(0.264-3.508)	0.954
Grade	I+II	0.647(0.264-1.583)	0.340	0.618(0.248-1.541)	0.302
	III+IV	0.844(0.631-1.129)	0.254	0.819(0.611-1.097)	0.180
Tumor stage	T1	1.019(0.564-1.841)	0.950	1.039(0.574-1.881)	0.900
	T2	0.775(0.566-1.062)	0.112	0.753(0.549-1.033)	0.078
No. Of LNs positive	1	1.080(0.739-1.580)	0.691	1.061(0.725-1.552)	0.761
	2	0.633(0.392-1.022)	0.061	0.657(0.405-1.065)	0.088
	3	0.423(0.190-0.941)	0.035	0.396(0.175-0.900)	0.027
Chemotherapy	no	0.163(0.019-1.402)	0.098	0.061(0.004-0.938)	0.055
	yes	0.866(0.654-1.146)	0.314	1.191(0.899-1.578)	0.224

LN= lymph node

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Effect of postmastectomy radiotherapy on T1-2N1M0 triple-negative breast cancer

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