Tissue- and Blood-Based mRNA Tests in Breast Cancer

Version	Summary	Created by	Modification	Content Size	Created at	Operation
1		Helena Sabina Čelešnik	--	3331	2023-02-14 11:00:43	\|
2	format change	Peter Tang	Meta information modification	3331	2023-02-15 01:58:01	\|

This entry is adapted from the peer-reviewed paper 10.3390/cancers15041087

Molecular diagnostic tests help clinicians understand the underlying biological mechanisms of their patients’ breast cancer (BC) and facilitate clinical management. Several tissue-based mRNA tests are used routinely in clinical practice, particularly for assessing the BC recurrence risk, which can guide treatment decisions. Blood-based mRNA assays have only recently started to emerge.

breast cancer peripheral blood diagnostic assay mRNA test transcriptome early detection cancer screening

1. Introduction

Breast cancer (BC) is the most diagnosed cancer in women, and among the leading causes of cancer mortality. It is estimated that over 86,000 European women will die of this disease in 2022 ^[1]^[2]. BC is a heterogeneous cancer comprised of distinct subtypes with specific pathological characteristics and clinical implications. Based on the expression of the estrogen receptor (ER), progesterone receptor (PR), and the amplification of the HER2 (ERBB2) receptor, BC is categorised into four clinical subtypes: hormone receptor (HR)-positive (ER+/PR+/HER2−), triple positive (ER+/PR+/HER2+), HER2-positive (ER−/PR−/HER2+), and triple-negative breast cancer (TNBC) (ER−/PR−/HER2−, also HR−/HER2−) ^[3]^[4]. This classification is clinically important, because it helps to assess cancer prognosis, and, in company with other traditional prognostic and predictive factors, select an appropriate treatment strategy. ER-positive tumours respond to drugs that target the ER pathway, such as the selective ER modulators and ER degraders (tamoxifen, fulvestrant) or aromatase inhibitors (letrozole, anastrozole, exemestane) ^[5]. Tumours with HER2 amplification respond to anti-HER2 therapies (i.e., monoclonal antibodies targeting HER2, such as trastuzumab and pertuzumab) ^[6]. However, TNBC does not express ER, PR, and lacks HER2 amplification, and therefore targeted therapies are lacking for this subtype, since targeted therapies are commonly aimed at these receptors. Consequently, TNBC represents a major clinical challenge, and is associated with a poor prognosis connected with metastasis, post-treatment relapse, and reduced survival. While the standard treatment for TNBC involves chemotherapy, new immunotherapy options have become available in recent years ^[7]^[8]. One important characteristic of TNBC is its high mutational burden ^[9]^[10], which is associated with tumour immunogenicity, and may aid in the selection of TNBC patients likely to benefit from certain immunotherapies ^[11]. Treatment decisions for this heterogeneous cancer may also be guided by RNA-based molecular subtyping. The web-based TNBCtype algorithm was developed as an online tool to distinguish six TNBC subtypes with different biological characteristics and therapy options ^[12]^[13].

In addition to the clinical subtyping of BC, a detailed molecular characterisation of BC tissues, which employed DNA analyses (DNA mutations, copy number, DNA methylation), mRNA profiling and protein expression of tumour tissues, has led to the classification of four molecular/intrinsic BC subtypes with different prognoses and survival: Luminal A (ER+/PR+/HER2−, low proliferation factor Ki67+, low grade), Luminal B (ER+/PR±/HER2±, high Ki67+ (≥14%), high grade), HER2-enriched (ER−/PR−/HER2+, high proliferation, any Ki67 level), and basal-like (ER−/PR−/HER2−, high proliferation, any Ki67 level, high grade, necrosis) ^[3]^[14]. Intrinsic and clinical subtypes overlap to some degree, but not completely. For instance, basal-like breast cancers are mostly enriched in TNBC. However, about 21% of TNBCs are not basal-like ^[15].

2. Molecular Diagnostic Tests and Companion Diagnostic Devices for Breast Cancer Approved by the US Food and Drug Administration (FDA)

The diagnostic tests available for BC are intended to detect variations in DNA sequence, analyse RNA profiles, or measure protein expression, in order to determine the genetic carrier status, classify BC and its subtypes, detect cancer spreading, facilitate prognosis, and/or assess recurrence risk. In clinical care, a number of nucleic acid-based tests have been adopted for BC in recent years. Some of them have been cleared or approved by the FDA ^[16]. These include multigene expression assays, tests for variant detection in BRCA1, BRCA2, PIK3CA, and Topoisomerase II Alpha genes, and assays for determination of HER2 status. In addition, a number of companion diagnostic devices for BC have been approved by the FDA ^[16]. These are in vitro diagnostic (IVD) devices and imaging tools that provide information needed for the safe and effective use of corresponding therapeutics. For BC, FDA-approved IVD devices include testing for BRCA 1, BRCA2, and PIK3CA mutations, HER2 gene amplification, and protein expression of HER-2, PD-L1, and Ki67. These DNA and protein-level tests facilitate decisions on therapy with Herceptin, Kadcyla, Perjeta, Lynparza, Talzenna, Piqray, Verzenio, and Keytruda. Some tests are classified both as a nucleic acid-based test and IVDs.

3. Cancer Diagnostics Based on mRNA Can Offer Prognostically Useful Information beyond DNA Variation

Messenger RNA diagnostics are able to provide important information that cannot be learned directly from mutation data ^[17]. For instance, although evaluating a predisposition to hereditary cancer using DNA genetic testing is becoming widespread, it can often be challenging to interpret the detected variants accurately, especially when DNA alterations are predicted to impact splicing. In these cases, the variants are frequently classified as uncertain, or likely pathogenic. However, RNA testing can help interpret the impact of these changes by enabling their classification as pathogenic/clinically actionable or benign ^[18], thereby informing clinical decisions. According to Karam et al., blood RNA testing provided as a supplement to DNA genetic testing has the potential to affect medical management in at least 1 in 43 patients ^[18].

Additionally, although hereditary BC risk has been linked to highly penetrant genetic variants, many of their carriers never develop BC, and many BC patients do not carry these variants ^[19]^[20]. This can create uncertainty for both the patients and the physicians when it comes to making decisions whether to pursue aggressive prevention strategies (e.g., prophylactic surgery, chemopreventive intervention). To get a more accurate assessment of individual risk, examining gene-expression patterns can make it easier to differentiate individuals from high-risk families who are likely to develop BC from those who are not ^[21]. This way, women who carry known susceptibility variants can be assigned different individual risks based on their gene expression profiles, which may facilitate personalised prevention decisions ^[21].

The clinical contribution of mRNA testing beyond that of DNA becomes particularly apparent in early-stage BC diagnosis and assessment of BC recurrence risk, which can guide treatment decisions ^[17]. For example, the 21-gene expression tissue assay Oncotype DX can identify pathway changes on a very detailed level, and predict recurrence within the HR-positive BC more precisely than any DNA-based assay ^[17]^[22]. While genomic mutations can lead to changes in the downstream pathways, there may be several intermediate steps between the driver mutations and the disease phenotype. However, distinct expression patterns that can result from the driver mutations can be identified easily by examining the mRNA levels. Consequently, mRNA analysis can be more informative than analysis of genomic variation.

While several tissue-based mRNA assays are used and/or FDA-approved, only a few blood-based mRNA tests (described below) are commercially available, and none have so far been approved by the FDA. Additionally, none of the current FDA-approved companion devices for BC are based on mRNA detection, either in blood or in tissues.

4. Tissue-Based mRNA Expression Assays for Breast Cancer

Tissue gene expression assays investigate the patterns of a selected number of different genes in cancer cells obtained during surgery or biopsy, to help inform clinical decisions (Table 1). For instance, several multigene prognostic assays (e.g., Oncotype DX, Prosigna, EndoPredict), enable estimation of the residual risk of recurrence following surgery. This can guide clinical decisions, such as whether chemotherapy or other treatments are needed to reduce risk after surgery. Consequently, this can facilitate safe avoidance of patient over-treatment.

4.1. Prosigna Breast Cancer Prognostic Gene Signature Assay (Formerly Called the PAM50 Test)

Prosigna (Veracyte, San Francisco, CA) is an FDA-approved test that uses a 50-gene expression profile of BC tumour tissue to inform prognostic, recurrence and therapeutic management of BC ^[23]^[24]^[25]^[26]. It is intended for post-menopausal women with stage I or II, lymph node (LN) negative or positive (1–3 positive LNs), hormone-receptor (HR)-positive BC, with a tumour size of <5.0 cm. Prosigna can help assign BC to one of four intrinsic subtypes and provide a risk assessment for distant recurrence at ten years. The results of this test, together with other clinical information, can be used by physicians for assessing the recurrence risk. Based on the low, intermediate or high risk of distant recurrence, physicians can decide if patients can safely avoid adjuvant chemotherapy ^[25]^[27].

4.2. MammaPrint Test (also Called the 70-Gene Signature)

MammaPrint (Agendia, Inc., Amsterdam, The Netherlands) is an FDA-cleared prognostic assay, which analyses the expression of 70 genes to help predict if BC will spread to other parts of the body or return ^[28]^[29]^[30]. Based on the calculated recurrence score, women are categorised into a high or low risk group, which can guide decisions on adjuvant endocrine and chemotherapy ^[28]^[31]. MammaPrint is performed on fresh or preserved tissues from biopsy or surgery, and is intended for early-stage invasive HR-positive or HR-negative, stage I or II cancers, smaller than 5.0 cm, present in three or fewer lymph nodes ^[32]. It can be integrated into diagnostic workups for quicker, more informed decisions on pre- and post-operative treatment. BluePrint, another assay by Agendia, Inc., is a molecular classification system that analyses 80 genes to identify the underlying biology of individual breast cancers. It enables BC subtyping into luminal type (luminal A or luminal B), HER2-type, and basal-like type. This classification reveals valuable information about long-term prognosis and response to systemic therapy, and can enable patient selection for either chemotherapy or endocrine treatment ^[33].

4.3. Oncotype DX Breast Recurrence Score Test

Oncotype DX (Genomic Health, Redwood City, CA, USA) ^[34] is a gene expression profiling assay intended for HR+/HER2− BC, stage I, II or IIIa, LN-negative, or up to three positive LNs. It analyses the expression of 21 genes in cancer cells obtained by biopsy or surgery, and helps assess the risk of BC recurrence. The calculated recurrence score enables an individualised estimate of 9-year distant recurrence risk and the likelihood of adjuvant chemotherapy benefit ^[35]^[36]. Oncotype DX became commercially available in 2004, and, as a laboratory-developed test, did not require FDA-approval ^[37]. The assay is included in international treatment guidelines, and is performed at a CLIA-certified central laboratory in the USA. It has been validated extensively in clinical studies. A large adjuvant BC treatment clinical trial (TAILORx, NCT00310180), which included 10,253 patients worldwide, demonstrated that, by using Oncotype DX, it is possible to identify BC patients who may not need chemotherapy to increase their chance of survival ^[37]^[38]^[39]^[40]^[41].

4.4. Breast Cancer Index, BCI

BCI (Biotheranostics, Inc., San Diego, CA, USA) is a predictive multi-gene expression assay that incorporates: (1) the HOXB13:IL17BR ratio, which is associated with tumour responsiveness to endocrine therapy; and (2) the molecular grade index, which is associated with tumour proliferation, and is based on the average expression of five cell cycle-associated genes ^[42]^[43]. BCI helps to predict the risk of early-stage HR+ BC coming back 5 to 10 years after diagnosis. According to the American Society of Clinical Oncology (ASCO) guidelines and NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines^®), this assay can also help physicians decide if extending hormonal therapy in patients with HR+/HER2−, LN-negative or LN-positive (1–3 nodes) BC beyond five years (for a total of 10 years) would be beneficial ^[31]. The clinical validation and the indication of prognostic utility for this molecular signature was provided by the TransATAC and the Stockholm trials ^[42]^[44].

4.5. EndoPredict Breast Cancer Prognostic Test

EndoPredict (Myriad Genetics, Salt Lake City, UT, USA) is a gene expression test for patients with early-stage, ER+/HER2− BC. It analyses 12 genes related to tumour proliferation and hormone receptor activity. It calculates a risk score, which can be used together with clinical pathological factors (such as tumour size and nodal status) to guide treatment decisions for chemotherapy and extended endocrine therapy ^[45]^[46]. It enables prediction of early and up to 15 years distant recurrence (metastatic disease) ^[47]^[48]^[49]. It has been validated clinically in both post- and pre-menopausal patients ^[50]^[51]. By using EndoPredict, it was possible to identify 65% of premenopausal patients with low-risk disease who could safely forgo adjuvant chemotherapy (independent from nodal status) ^[51].

4.6. GeneSearch Breast Lymph Node (BLN) Test Kit

GeneSearch BLN (Veridex, LLC., Raritan, NJ, USA) is an FDA-approved gene expression test for patients with invasive BC, intended to detect whether BC cells have spread to lymph nodes under the arm ^[52]. The assessment is based on the analysis of two gene expression markers, mammaglobin (MG) and cytokeratin 19 (CK19) in lymph node(s) removed during surgery. These mRNA markers are expressed at high levels in breast tissue, but only at low levels in normal lymph node tissue (i.e., cell-type-specific mRNAs) ^[53]^[54]^[55]^[56]. Metastases greater than 0.2 mm can be detected by the BLN Test in nodal tissue removed from sentinel lymph node biopsies, and the assay results can be used to guide the decision to remove additional lymph nodes ^[52].

Table 1. Tissue mRNA-level diagnostic tests for breast cancer.

Assay Trade Name (Manufacturer)	Number of Genes; Sample Type	Assay Indicated For	Description	Methodology/ Platform	FDA Numbers; References
Prosigna Breast Cancer Prognostic Gene Signature Assay (Veracyte, Inc.)	50 genes; BC tissue (formalin-fixed paraffin embedded—FFPE)	HR+, LN-negative or 1–3 positive nodes, stage I or II cancers	Classification of intrinsic BC subtypes; prognostic; recurrence risk assessment; guides adjuvant endocrine and chemotherapy in postmenopausal patients	nCounter Dx Analysis System (mRNA hybridization to DNA probes)	FDA (K130010); ^[26]^[31]
MammaPrint (Agendia, Inc.)	70 genes; BC tissue (FFPE or fresh)	HR+ or HR−, LN-negative or 1–3 positive nodes, stage I or II cancers, ≤5.0 cm	Prognostic; recurrence risk assessment; guides adjuvant endocrine and chemotherapy in patients >50 or postmenopausal patients	Microarray-based assay; also available as a targeted RNA next-generation sequencing assay	FDA (K101454, K081092, K080252, K070675); ^[31]^[57]^[58]
Oncotype DX Breast Recurrence Score Test (Genomic Health)	21 genes (16 cancer-related and 5 reference genes); BC tissue (FFPE)	HR+/HER2−, LN-negative or 1–3 positive nodes, stage I, II or IIIa cancers, ≤5.0 cm	Prognosticates distant recurrence; predicts chemotherapy benefit/guides adjuvant endocrine and chemotherapy in postmenopausal or premenopausal patients	qRT-PCR-based assay	^[31]^[34]^[35]^[36]^[59]
Breast Cancer Index—BCI (Biotheranostic, Inc.)	7 genes; BC tissue (FFPE)	HR+, LN-negative or 1–3 positive nodes, stage I–III cancers, invasive BC cases without evidence of recurrence	Prognosticates risk of distant recurrence; predicts likelihood of benefit from extended (>5 years) endocrine therapy; guides adjuvant endocrine and chemotherapy in patients >50 or postmenopausal patients	qRT-PCR-based assay	^[31]^[60]
EndoPredict (Myriad Genetics)	12 genes (8 BC-related and 4 reference genes); BC tissue (FFPE)	HR+/HER2−, LN-negative or 1–3 positive nodes, tumour size T1–T3, grade 1–3	Predicts distant recurrence at 10 years (and up to 15 years); guides adjuvant endocrine and chemotherapy in patients >50 or postmenopausal patients; identifies premenopausal patients who do not need chemotherapy	qRT-PCR-based assay	^[31]^[46]^[61]
GeneSearch Breast Lymph Node (BLN) Test Kit (Veridex, LLC.)	3 genes (2 metastasis-related and 1 reference); lymph node(s) removed during surgery	Patients with invasive BC, scheduled for sentinel lymph node dissection	BC metastasis detection	qRT-PCR-based assay	FDA: P060017 S001–S004, ^[52]

5. The Advantages of Using Peripheral Blood (i.e., a Blood-Based Liquid Biopsy) for Cancer Diagnostics

Cancer biomarker research has concentrated largely on the molecular characteristics of tumour cells, and on immune responses in the tumour microenvironment, leading to the emergence of tissue-based diagnostic assays. However, focusing on blood biomarkers has many advantages for cancer screening, diagnosis, monitoring, and prognosis.

First, drawing peripheral blood offers simple, cost-effective and minimally invasive sampling. Additionally, it is well known that patient survival rates are greatly increased if cancer is identified at its early stages ^[62], and several lines of evidence indicate that analysing blood allows the detection of very early systemic changes, which is crucial for cancer screening ^[63]^[64]^[65]^[66]. On the other hand, biopsies may not be appropriate for cancer screening, and may deter healthy people with no symptoms ^[67]. Currently, almost 50% of cancers are diagnosed at the later stages, when the symptoms begin to manifest. At that time, the disease outcomes are poorer and the treatments more expensive ^[68]. The less invasive blood sampling may make early cancer detection and accompanying medical intervention more feasible. A liquid biopsy may also offer advantages compared to the existing imaging methods. About half of women have dense breast tissue, which is associated with reduced sensitivity on mammography ^[69]. Additionally, the tumour has to reach a certain size to be detectable by imaging ^[70]. Moreover, although close to 20% of patients with invasive BC are women under 50, in some countries, women in this age group are not typically referred for mammography screenings ^[71]. A liquid biopsy could represent a solution to these issues.

Although repeated tissue biopsies can be useful in clinical practice to help monitor how the tumour evolves, tissue collection comes with risk of complications ^[66]. It may also provide insufficient material, and can have selection bias due to tumour heterogeneity (e.g., single-site tissue biopsies may give only a snapshot of the tumour) ^[72]. In contrast, peripheral blood is readily available, and not prone to selection bias or heterogeneity problems.

Since blood testing has the potential to circumvent all the above-mentioned disadvantages of biopsies and imaging, liquid biopsy has been gaining considerable interest in BC precision medicine. A variety of biomarkers with clinically useful information can be detected in blood, such as circulating tumour cells (CTCs), circulating tumour-derived material (e.g., circulating tumour DNA—ctDNA), extracellular vesicles, cell-free microRNAs (cfmiRNAs), methylation markers, and others. These have been reviewed in several excellent papers, e.g., ^[73]^[74]^[75]^[76]^[77]. Here, the researchers will focus on mRNA biomarkers from peripheral blood cells and their use in cancer diagnostics.

6. Research Focusing on BC-Specific Transcriptional Profiles in Peripheral Blood Has Established Their Diagnostic and Prognostic Value

During cancer, the proportion of effector and regulatory immune cells and their gene expression profiles change in the tumour microenvironment. Similar immune changes can be detected in peripheral blood cells, since the circulatory system participates in physiological and pathological activities throughout the body ^[78]^[79]. Tumours release a variety of signalling molecules that are detected by the circulating blood cells. These respond with phenotypic and functional changes that enable them to modulate the cancer’s progression. This can result either in the killing of tumour cells and cancer rejection, or the promotion of cancer proliferation and spreading ^[80]^[81]^[82].

In recent years, high-throughput transcriptomic studies have revealed meaningful differences in peripheral blood cells between BC and healthy subjects, and within BC patient subpopulations. Specific transcriptome changes have been identified with clinical utility for BC patients, indicating a clear potential for liquid biopsy and the development of blood-based messenger RNA diagnostic tests ^[83]^[84]^[85].

7. Commercially Available Blood-Based mRNA Tests for Breast Cancer

Currently, blood analysis in clinical management of BC is aimed mostly at detecting DNA-level and protein-level biomarkers. Examples include the BRCA1 and BRCA2 genes, which are the classical blood-based biomarkers for genetic screening of individuals with hereditary BC susceptibility ^[86]. Other blood BC biomarkers include proteins that can help assess disease progression, predict recurrence, and facilitate the monitoring of treatment response, such as carcinoembryonic antigen (CEA), gene products of MUC1 (e.g., cancer antigen (CA) 15-3 and CA 27.29), circulating cytokeratins, and serum HER2 ^[87]^[88].

However, recent years have brought a gradual emergence of mRNA-level blood diagnostics, with new mRNA assays finding their way increasingly into the clinical setting (Table 2). As detailed below, these blood tests can facilitate healthcare decisions in several ways; by supplementing hereditary DNA-testing for better diagnostic outcome (i.e., helping to classify DNA variants) (+RNAinsight), by enabling early BC detection (Syantra DX Breast Cancer, BCtect), and by facilitating simultaneous screening of several cancers (multi-cancer blood test Aristotle).

Table 2. Commercially available blood mRNA-level diagnostic tests for breast cancer.

Assay Trade Name (Manufacturer)	Number of Genes	Assay Indicated for	Description	Methodology/ Platform	References
+RNAinsight (Ambry Genetics)	Up to 91 genes (for maximum coverage)	Assessing hereditary cancer predisposition	+RNAinsight analyses functional RNA data to classify DNA variants and identify deep-intronic mutations; intended for paired RNA/DNA analyses, as a supplement to Ambry Genetics DNA-level hereditary cancer panels CancerNext, CancerNext-Expanded, CustomNext-Cancer.	RNA sequencing	^[89]
Syantra DX Breast Cancer (Syantra Inc.)	12-gene multi-biomarker panel	Breast cancer screening for women aged 25–80	Enables classification of a sample as positive or negative for BC signature; demonstrated utility for early cancer screening, for women with high breast density, and for women under 50.	qRT-PCR-based assay	^[90]^[91]
Multi-cancer blood test Aristotle (Stage Zero Life Sciences Ltd.)	Multi-biomarker panel	Pan-cancer screening (breast, bladder, colorectum, cervix, endometrium, liver, ovary, prostate, and stomach)	Enables detection of multiple cancer molecular signatures from a single blood sample (early cancer detection).	Microarray-based assay	^[92]
BCtect (DiaGenic ASA)	96-assay signature	Breast cancer screening	Enables classification of a sample as positive or negative for BC signature; utility for early BC detection in both pre- and post-menopausal women, and across cancer stages and types.	qRT-PCR-based assay	^[93]^[94]^[95]

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