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Yang, T.; Li, W.; Huang, T.; Zhou, J. Genetic Testing for Early-Stage Breast Cancer. Encyclopedia. Available online: https://encyclopedia.pub/entry/52529 (accessed on 02 July 2024).
Yang T, Li W, Huang T, Zhou J. Genetic Testing for Early-Stage Breast Cancer. Encyclopedia. Available at: https://encyclopedia.pub/entry/52529. Accessed July 02, 2024.
Yang, Tinglin, Wenhui Li, Tao Huang, Jun Zhou. "Genetic Testing for Early-Stage Breast Cancer" Encyclopedia, https://encyclopedia.pub/entry/52529 (accessed July 02, 2024).
Yang, T., Li, W., Huang, T., & Zhou, J. (2023, December 08). Genetic Testing for Early-Stage Breast Cancer. In Encyclopedia. https://encyclopedia.pub/entry/52529
Yang, Tinglin, et al. "Genetic Testing for Early-Stage Breast Cancer." Encyclopedia. Web. 08 December, 2023.
Genetic Testing for Early-Stage Breast Cancer
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This entry is adapted from the peer-reviewed paper 10.3390/ijms242316607

Early-stage breast cancer refers to breast cancer at clinical stage I–stage II, accounting for 73.1% of breast cancer. For patients at an early stage, rational and effective treatment is vital to improve prognosis. An increasing number of studies have made important progress, such as the OlympiA trial of adjuvant olaparib in patients with germline pathogenic variants in BRCA1/2 and the KARISMA trial of CYP2D6 mutations in patients using tamoxifen. Regimens of adjuvant and neoadjuvant treatments used to be mainly based on the clinicopathological characteristics of patients, but deficiencies are still noticed in forecasting the efficacy and prognosis. To complement the deficiency, MGAs, including Oncotype Dx, MammaPrint, RecurIndex, BCI, EndoPredict, and PAM50, were developed.

breast cancer precision diagnosis treatment genetic testing

1. Oncotype Dx

Oncotype Dx, which is also called the 21-gene recurrence score (RS) assay, is an MGA for HR-positive HER-2-negative breast cancer patients that evaluates RS. Its capacity to predict prognosis and benefit from adjuvant chemotherapy or radiotherapy has been explored in breast cancer patients at stages N0–N1. The Oncotype Dx is relatively widely used in Europe and America. The 21 genes involved in Oncotype Dx were established from the NSABP B-14 study, which investigated the expression of 250 genes in 666 HR-positive node-negative breast cancer patients in the early stage. The risk of recurrence was initially divided into low (RS < 18), intermediate (18 ≤ RS < 31), and high (RS ≥ 31), according to RS [1]. Since RS proved to be an independent risk factor for the prognosis of HR-positive breast cancer patients, further study NSABP B-20 aimed to validate the predictive value of Oncotype Dx in chemotherapy sensitivity. Patients in the high-risk group tend to benefit from adjuvant chemotherapy, while patients in the low-risk group are deemed to have little benefit from chemotherapy. Although the benefit of chemotherapy is unclear for patients in the intermediate group, these patients may also benefit from chemotherapy in clinical practice [1][2]. The phase III trial TAILORx confirmed the value of predicting the efficacy of chemotherapy and prognosis that Oncotype Dx possesses. The risk threshold was reclassified as low risk (RS < 11), intermediate risk (11 ≤ RS < 26), and high risk (RS ≥ 26). HR-positive breast cancer patients in the intermediate-risk group were randomized to receive either endocrine therapy or endocrine therapy plus chemotherapy. There was no significant difference in invasive disease-free survival (iDFS) and overall survival (OS) between the endocrine therapy group and the chemoendocrine therapy group. However, adjuvant chemotherapy markedly reduced 9-year distant recurrence in patients younger than 50 years old. Adjuvant chemotherapy decreased rates of distant recurrence in patients with RS of 16 to 20 and 21 to 25 by 1.6% and 6.5%, respectively. Therefore, for patients in the intermediate-risk group, those who are younger than 50 and with RS ranging from 16 to 25 are more likely to benefit from chemoendocrine therapy [3][4].
The prognostic significance of Oncotype Dx for HR-positive breast cancer patients with lymph node metastasis was also explored by some clinical trials. The SWOG S8814 study analyzed 367 postmenopausal patients and revealed that higher RS was linked with a worse prognosis for patients who received endocrine therapy only. In addition, high-risk patients defined by RS could benefit from chemotherapy [5]. Another phase III study, RxPONDER, also investigated Oncotype Dx in HR-positive patients at stage N1 with RS less than 25. Patients received endocrine therapy with or without chemotherapy. Premenopausal patients were proved to benefit from chemotherapy, but the benefit was not positively associated with RS. Of note, patients with more than or equal to two positive lymph nodes only took up 34% in this study. Whether the conclusion can be applied to patients with multiple lymph node metastases needs to be further explored [6].
The WSG-ADAPT-HR+/HER2− trial is the initial study to assess the combination of RS and response to neoadjuvant endocrine therapy as an indication of regimens. Ki-67 was tested before and after neoadjuvant endocrine therapy to reflect the response. Patients with RS ranging from 12 to 25 and without endocrine therapy response received adjuvant chemotherapy as the experimental arm, while other patients with RS less than 25 were taken as the control arm. For low-risk patients and patients that respond to neoadjuvant endocrine therapy, endocrine therapy also was not inferior to endocrine therapy plus chemotherapy [7]. In addition, combining RS with response to endocrine therapy is a practicable strategy to guide systemic treatment for HR-positive breast cancer patients with less than three positive lymph nodes [8][9].
Oncotype Dx has been shown to predict the efficacy of adjuvant radiotherapy by analyzing RS and local-regional recurrence (LRR). In the NSABP B-28 study, 10-year LRR increased with the increased risk that was demonstrated by the RS. Further, RS was defined as an independent risk factor of LRR [10]. Another study also revealed that increased RS was associated with increased LRR rates through genetic testing in 316 HR-positive breast cancer patients [11]. Taken together, Oncotype Dx can contribute to the selection of adjuvant radiotherapy by indicating LRR risks in node-positive patients.

2. MammaPrint

MammaPrint, also known as the 70-gene risk of distant recurrence signature, is an MGA developed for HR-positive HER-2-negative breast cancer patients in stage N0–N1 [12]. Similar to Oncotype Dx, MammaPrint predicts the risk of recurrence and metastasis, as well as indicating treatment management. Using DNA microarray techniques, the MammaPrint tests 70 genes and divides patients into high-risk and low-risk groups. A phase III study, MINDACT, enrolled 6693 breast cancer patients whose genomic risk and clinical risk were assessed through the use of MammaPrint and Adjuvant! Online, respectively. Chemotherapy was prescribed for those who were found to have a high genomic and clinical risk, whereas those with a low risk for both were not given chemotherapy. Patients with controversial genomic risks and clinical risks were randomly assigned to chemotherapy or the control group, and there were no significantly different 5-year distant metastasis-free survival (DMFS) rates between these two groups, indicating that MammaPrint can exempt approximately 46% of clinically high-risk patients from chemotherapy. Patients at both low risks showed the best prognosis, while patients at both high risks benefit from chemotherapy [13]. The results from the 8-year follow-up and subgroup analysis of the MINDACT trial demonstrated that patients who are younger than 50 years old and have distinct genomic and clinical risks may achieve therapeutic effects from chemotherapy [14].

3. RecurIndex

RecurIndex is employed in N0–N2 stage HR-positive breast cancer patients to direct adjuvant therapy. The 28 genes tested in RecurIndex were established to indicate the risk of distant metastasis in Asian patients, as well as estimate the benefit from adjuvant chemotherapy or radiotherapy. To verify the RecurIndex, a total of 752 operable breast cancer patients were enrolled and divided into high-risk and low-risk groups by RecurIndex. The 10-year relapse-free survival (RFI) for high-risk and low-risk groups was 80.5% vs. 90.0%, and the 10-year distant RFI was 85.0% vs. 94.1%. Subgroup analysis noted a modest chemotherapy benefit in the high-risk group [15]. Another study conducted using 490 HR-positive patients also revealed a significant difference in distant RFI between high-risk and low-risk groups, regardless of lymph node metastasis [16]. The results taken from RecurIndex were proven with prognostic values, which may be conducive to the decision concerning adjuvant chemotherapy.
Further validation research has investigated the predictive role of RecurIndex in adjuvant radiotherapy. A total of 388 patients at clinical stage I–III were followed up, and 10-year local RFI was analyzed. Local RFI was 100% in both the radiotherapy group and the control group for low-risk patients defined by RecurIndex, while radiotherapy improved local RFI at 18.2% for high-risk patients [17]. For stage N1 breast cancer patients, low-risk patients in the RecurIndex test showed no statistical difference in local RFI, distant RFI, recurrence-free survival (RFS), and overall survival (OS) between those who underwent adjuvant radiotherapy and those who did not. High-risk patients who received radiotherapy showed markedly higher distant RFI, local RFI, RFS, and OS [18]. Thus, decision making concerning adjuvant radiotherapy can be guided by RecurIndex, wherein high-risk patients in stage N1 are recommended to undergo radiotherapy to prevent recurrence.

4. BCI

The BCI was developed for postmenopausal HR-positive node-negative breast cancer patients. To predict prognosis and the response to endocrine therapy, 11 genes, including four reference genes were detected. The results of BCI provide scores for five progression-related genes and the ratio of HOXB13 to IL17BR (H/I), which are genes involved in the estrogen signaling pathway [19][20][21][22]. The Trans-aTTOM trial investigated patients, of which 49% are defined as high risk by BCI (H/I). Compared with patients who received tamoxifen (TAM) for 5 years, patients who received TAM for 10 years showed increased RFI in the high-risk group. In contrast, low-risk patients did not benefit from extended endocrine therapy, demonstrating that patients with elevated BCI can benefit from extended endocrine therapy. The association between BCI and prolonged endocrine therapy stayed present even after eliminating confounding factors, including pathological features [23][24]. The IDEAL study confirmed the benefit of additional letrozole treatment for 5 years compared with an additional 2.5 years. Both clinical high-risk and BCI high-risk patients received better RFI in those who received additional 5-year letrozole. For BCI low-risk patients, no statistical difference was noticed between extending letrozole for 5 years and 2.5 years, regardless of what level of the clinical risk [25]. Extended endocrine therapy was advised for BCI high-risk patients owing to the increased risk of distant recurrence.

5. EndoPredict

The EndoPredict test combines the expression of 12 genes and clinicopathological features, including tumor size and lymph node metastasis, to rate an EPclin score that indicates prognosis. EPclin score can divide ER-positive HER-2-negative patients into the high-risk group and the low-risk group, hence indicating the risk of recurrence and adjuvant therapy regimens [26]. The ABCSG-6/8 cohorts evaluated EPclin score in postmenopausal ER-positive patients who were administered endocrine therapy only and investigated their distant recurrence-free rate (DRFR). Patients with low EPclin scores showed significantly higher DRFR in both node-positive and node-negative subgroups, validating the prognostic value of EndoPredict [27]. Subsequently, the association of high-risk EPclin scores and worse distant recurrence-free survival (DRFS) in premenopausal patients was revealed via retrospective analysis [28]. The promising predictive role of EndoPredict promoted its exploration in forecasting chemotherapy benefits. A study enrolled 373 ER-positive breast cancer patients with 0–3 metastatic lymph nodes. The 3-year disease-free survival (DFS) was increased by 4.8% (96.3% vs. 91.5%) in high-EPclin score patients who received chemotherapy, confirming the predictive value of EndoPredict in adjuvant chemotherapy benefit [29].

6. PAM50 Risk of Recurrence (ROR)

The PAM50 assay was designed to classify the intrinsic molecular subtype of breast cancer and differs from other MGAs. It detects 50 oncogenic genes and five reference genes and categorizes breast cancers into luminal A, luminal B, HER-2-enriched, and basal-like subtypes [30]. Potential effective agents were explored for different subtypes in the NCIC.CTG MA.5 trial and NCIC.CTG MA.12 trial, indicating the efficacy of anthracycline for the HER-2-enriched subtype and tamoxifen for luminal subtypes [31][32].
The risk of recurrence (ROR) score was generated, which concluded the results of the PAM50 assay and tumor size. The role of predicting the prognosis that PAM50 subtyping and ROR score possessed was also proved in NCIC-MA.5 and NCIC-MA.12 trials [33]. In a separate trial, patients with low ROR scores and no positive lymph nodes demonstrated optimal outcomes even without receiving adjuvant therapy. This highlights the ROR’s predictive value in prognosis and chemotherapy benefits [34]. The predictive power of ROR, Oncotype Dx, EndoPredict, and BCI was compared in the transATAC study. A total of 785 patients were analyzed, and connections were revealed between the four MGAs. However, Oncotype Dx was found to be stronger in estrogen-related modules, while ROR, BCI, and EndoPredict are more persuasive in proliferative-related genes [35].
Besides results from transATAC, there exist differences between the MGAs for early-stage breast cancer. The applicable populations vary from MGAs. The Oncotype Dx, MammaPrint, BCI, and EndoPredict are applicable for HR-positive HER-2-negative breast cancer patients at stage N0–N1, while RecurIndex is for HR-positive patients at stage N0–N2. PAM50, however, can be used for newly diagnosed breast cancer regardless of molecular subtypes. The genes selected for genetic testing in each MGA are also different. For instance, the status of ER, PR, HER-2, and Ki-67 are not included in the MammaPrint, and whether there exist positive lymph nodes is not stratified. The above information on molecular subtyping was included in the PAM50. Due to the different emphasis of each MGA, the choice of genetic testing should be individualized. Further, RecurIndex was established based on Asian populations, while other MGAs are based on European and American populations. The predictive value across different populations needs further exploration. The gene numbers, applicable populations, and representative trials are summarized, as shown in Table 1.
Table 1. Genetic testing for early-stage breast cancer.
MGAs Gene Number Detection Method Applicable Population Representative Trials Applications
Oncotype Dx 21 RT-PCR HR-positive HER-2-negative NSABP B-14 Predict prognosis,
      breast cancer, Stage N0–N1 NSABP B-20 Direct adjuvant chemotherapy or radiotherapy
        TAILORx  
        SWOG S8814  
        RxPONDER  
        WSG-ADAPT-HR+/HER2−  
        NSABP B-28  
MammaPrint 70 DNA-Microarray HR-positive HER-2-negative breast cancer, Stage N0–N1 MINDACT Predict the risk of recurrence and metastasis
RecurIndex 28 RT-PCR HR-positive HER-2-negative breast cancer, Stage N0–N2 Validation Researches Direct adjuvant chemotherapy or radiotherapy
BCI 11 RT-PCR HR-positive HER-2-negative Trans-aTTOM Predict prognosis,
      breast cancer, Stage N0–N1 IDEAL Predict response to endocrine therapy
EndoPredict 12 RT-PCR HR-positive HER-2-negative ABCSG-6 Predict prognosis
      breast cancer, Stage N0–N1 ABCSG-8  
PAM50 55 RT-PCR nCounter Newly diagnosed breast cancer NCIC.CTG MA.5 Classify the intrinsic molecular subtype,
        NCIC.CTG MA.12 Predict the risk of recurrence
        transATAC

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Tinglin Yang
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Wenhui Li
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Tao Huang
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Jun Zhou
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