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What’s New in Genetic Testing for Cancer Susceptibility?: Page 2 of 2

  • Jennifer K. Plichta, MD
  • Molly Griffin, BA
  • Joseph Thakuria, MD
  • Kevin S. Hughes, MD
September 15, 2016
Volume: 
30
Issue: 
9
  • Oncology Journal, Cancer and Genetics
Oncology (Williston Park). 30(9):787–799.
Table 1. Select Laboratories Offering BRCA Testing (Not Comprehensive)
Figure 1. Promises of the Genomic Age
Table 2. Summary of Select Gene Mutations With Associations of Various Cancer Susceptibilities
Figure 2. Summary of Select NCCN Management Strategies for Breast and Ovarian Cancer, Based on Genetic Test Results
Table 3. Summary of Select Studies of Cancer Patients Reporting Gene Mutations From Panel Testing Performed Concurrently With (‘Pre’) or After (‘Post’) BRCA Testing, With Cumulative Results Reported
Figure 3. Cumulative Proportions of Gene Mutations Represented in Results From Panel Testing of Select Cancer Patient Populations
Table 4. Selected Examples of NCCN Guidelines on When to Screen With BRCA1/2 Testing

Abstract / Synopsis: 

The advent of next-generation sequencing, and its transition further into the clinic with the US Food and Drug Administration approval of a cystic fibrosis assay in 2013, have increased the speed and reduced the cost of DNA sequencing. Coupled with a historic ruling by the Supreme Court of the United States that human genes are not patentable, these events have caused a seismic shift in genetic testing in clinical medicine. More labs are offering genetic testing services; more multigene panels are available for gene testing; more genes and gene mutations are being identified; and more variants of uncertain significance, which may or may not be clinically actionable, have been found. All these factors, taken together, are increasing the complexity of clinical management. While these developments have led to a greater interest in genetic testing, risk assessment, and large-scale population screening, they also present unique challenges. The dilemma for clinicians is how best to understand and manage this rapidly growing body of information to improve patient care. With millions of genetic variants of potential clinical significance and thousands of genes associated with rare but well-established genetic conditions, the complexities of genetic data management clearly will require improved computerized clinical decision support tools, as opposed to continued reliance on traditional rote, memory-based medicine.

More Interest in Gene Testing

Although commercial genetic testing has been available for over 20 years, uptake has been slow and compliance with guidelines has been marginal. It is estimated that more than 90% of unaffected BRCA carriers remain unaware of their status and are mismanaged.[26] Based on National Comprehensive Cancer Network (NCCN) guidelines for breast cancer,[18] millions of women are eligible for BRCA1/2 testing, and similar numbers of men and women are likely eligible for testing for other syndromes, most of whom are unaware of their eligibility.[27] Furthermore, using existing testing guidelines, it has been estimated that up to 50% of BRCA1/2 carriers may be missed as a result of arbitrary factors, such as small family size, higher male-to-female ratio in the family, and nonpaternity (all of which skew family histories to be interpreted as negative).

Why have we been failing? Providers often do not refer patients who need testing, either because there is insufficient time to take a thorough family history, because they lack the genetics expertise to analyze the histories they do take, or because they are unfamiliar with the genetic testing guidelines. It is well known that primary care physicians often do not have time to take a thorough family history,[28] and even oncologists are not taking thorough family histories from cancer patients.[29] Whether due to lack of expertise, lack of time, or lack of resources, many patients are never referred for testing.

On May 14, 2013, Angelina Jolie wrote an article in the New York Times chronicling her experience with breast cancer, genetic testing, and prophylactic surgery.[30] She revealed that she was diagnosed with a BRCA1 mutation and chose to have bilateral mastectomies to significantly reduce her risk of developing and dying from breast cancer. After sharing her story and decision to have prophylactic surgery, the medical community began to notice an increase in other women choosing to have bilateral mastectomies, although not always for the same reasons. This phenomenon has become known as the “Angelina Jolie effect.” To assess the potential impact of the “Angelina Jolie effect,” Evans et al reviewed breast cancer family history referral data from 2012 to 2013 in the United Kingdom, and reported a significant rise in breast cancer family history referrals, demand for BRCA1/2 testing, and inquiries regarding risk-reducing mastectomies.[31] Although awareness of Ms. Jolie’s story has become prevalent, improved understanding has not followed. In a follow-up report, Evans et al published ongoing breast cancer family history referral data that confirmed a persistent increase in bilateral risk-reducing mastectomies among women with and without genetic mutations, noting that the effect was greater in those without a BRCA1/2 mutation.[32]

However, patients are not the only ones missing key information. A patient-survey study from 2013 by McCarthy et al evaluated the rates and predictors of physician recommendations for BRCA1/2 testing among patients with breast cancer.[33] They reported that physician recommendations for BRCA1/2 testing were strongly associated with one’s risk of carrying a mutation, although only 53% of high-risk women reported a testing recommendation. Brown et al reported similar results with a web-based survey of women with early-onset breast cancer, which revealed that only 53% of women with a family history of cancer had been referred to see a genetic counselor, although 81% of Ashkenazi Jewish women had received a referral.[34] Even in a cohort of young women (≤ 40 years old) with breast cancer, Ruddy et al demonstrated that only 24% had undergone genetic testing.[35] These studies highlight a serious problem—namely, that many women who meet criteria for testing may not receive a recommendation for testing from their physician. On analysis of the results of a survey on family history of breast and ovarian cancer and BRCA testing, Vig et al reported that age at diagnosis, Jewish ancestry, and both maternal and paternal family history were strongly predictive of undergoing BRCA testing, likely due to the “high-risk” nature of these features, although age appeared to be more influential than family history in the older population.[36]

Unfortunately, many testing gaps are likely the result of a lack of education. In a national survey of primary care physicians that analyzed physician knowledge on BRCA testing, physicians were asked to select indications for BRCA testing from multiple clinical scenarios.[37] Overall, only 19% correctly selected all of the increased-risk and none of the low-risk scenarios. In a separate study of primary care providers and breast cancer risk assessment, Guerra et al reported that only 18% of physicians had used a software program to calculate breast cancer risk, even though 48% had ordered or referred a patient for BRCA1/2 testing.[38]

To address some of these disparities, Christianson et al conducted three focus groups including a total of 16 primary care providers to obtain input regarding the incorporation of a family health history risk assessment tool into a community healthcare system.[39] In this study, physicians identified their impediments as including deficiencies in the following areas: standard screening guidelines, effective screening tests, genetic counseling resources, and services for high-risk patients. In addition, the providers were concerned about their level of expertise, the cost of preventive healthcare, and genetic discrimination. These findings highlighted the need for consultation and referral services, evidence-based recommendations, and educational resources. Similar focus groups conducted by Sabatino et al also reported “lacking confidence in knowledge of risk and risk assessment” as one of the most common barriers to risk assessment, even though almost all providers agreed that assessing breast cancer risk was a primary care provider’s responsibility.[40]

Fortunately, things are changing. There is increasing interest in genetic testing among both clinicians and patients. As its cost goes down, as clinicians become more comfortable with its use, and as it is more openly discussed in the lay press, an increasing number of patients are undergoing testing. Rosenberg et al recently reported that the rate of genetic testing of women diagnosed with breast cancer at ages ≤ 40 was increasing annually, with 95.3% of such women tested in 2013.[41]

Unfortunately, this success also highlights a failure. Why were these women not identified and tested before they developed breast cancer? We tend to agree with Mary Claire King, who stated, “To identify a woman as a carrier only after she develops cancer is a failure of cancer prevention.”[42] It is hoped that the increase in the testing of cancer patients will be accompanied by a similar, although likely less dramatic, increase in the testing of unaffected women, and women who are diagnosed with breast cancer after the age of 40.

To do better, family histories must be taken and analyzed at the primary care level, and testing must be performed liberally. In addition, a concerted effort must be made to test every blood relative of any known mutation carrier. We must capitalize on the increasing medical and public interest in genetic testing and use every means possible to identify patients before they develop cancer. Although the primary care providers are one part of the solution, it is also clear that better support systems need to be developed to help physicians perform these assessments with efficiency and accuracy, and they need to be developed now.

More to Cover in Counseling

The American Society of Clinical Oncology (ASCO) has set the standard for counseling patients about genetic testing; their recommendations regarding elements of the genetic testing process requiring informed consent were recently updated to take into account panel testing.[43] Providing for informed consent for the first of these elements (“information on specific genetic mutation(s) or genomic variant(s) being tested”) seems impractical with the availability of panels of 20-plus genes, as it does for the second element (“implications of a positive or negative test”). It would be impossible to describe the 20-plus different genes to be tested in advance of testing, as well as the implications of a positive result for each test. The time commitment seems unnecessarily excessive, and the likelihood of the patient retaining useful information seems minimal. The solution suggested in the ASCO update[43]—“that genes be ‘batched,’ that high penetrance syndromes should be described, and that special attention should be paid to less penetrant genes and less well understood syndromes”—does not seem to fix this problem, since it still recommends that a large amount of information be provided prior to testing.

Genetic counseling today takes a significant amount of time per patient. McPherson et al estimate that it takes a genetics professional around 7 hours, on average, to counsel a new patient.[44] This estimate may be too high or may reflect time spent in research, but given that the average cancer genetic counselor sees 10 patients per week, this translates to 4 hours per patient in a 40-hour week. If counselors are expected to discuss all high-penetrance syndromes, less-penetrant syndromes, and less-understood syndromes associated with all the genes in a panel, this time commitment will only increase. The solution may well lie in changing our model of counseling. Perhaps in the current era it would be better to test patients with minimal pretest counseling, and then follow up with intensive counseling for those who test positive for a deleterious mutation or who have a VUS. Currently, less than half of genetic testing is being ordered by genetics professionals in the United States, with lack of clinician recommendation cited as a reason for not seeing a genetic counselor.[45] The solution is not clear, and there are strong opinions on both sides of this question. However, we must make a decision as to whether we should continue to give extensive counseling to a small number of patients or make genetic testing more broadly available to the millions of individuals who need it by truncating the pretest counseling component.[46]

Renewed Interest in Population Screening

There is renewed interest in population-level screening for cancer-causing mutations, since many patients with mutations do not meet criteria for testing under NCCN guidelines (Table 4).[18] These patients will not be found until after they develop cancer, exemplifying the “failure of prevention” noted by King.[42] She suggests: “…it is time to offer genetic screening of these genes [BRCA1 and BRCA2] to every woman, at about age 30, in the course of routine medical care.”[42] Although many experts may recoil in horror at this suggestion, we should step back and determine objectively why this is or is not a good idea.

Population-based screening for other genetic diseases is already being done for every baby born in this country under newborn screening guidelines.[47] Our hesitancy to extend population screening for cancer to adults stems back to a time when genetic testing was too expensive, when genetic tests were limited to single genes or syndromes, when choosing the appropriate test required tremendous expertise, and when adults with a genetic cancer predisposition had few options. Today, genetic testing is inexpensive, panel testing is ubiquitous, and management strategies exist to find cancers at an earlier and more treatable stage. Furthermore, there is increasing recognition of wide phenotypic spectra for any given mutation, which may have some overlap with other hereditary syndromes. Thus, when we do a panel test that includes a colorectal cancer gene in a patient with a suspected hereditary breast cancer, we are in many ways doing population-based screening, which might be defined as screening an individual for a cancer gene that is otherwise not suspected on the basis of their family history.

The near future is being tested at Boston Children’s Hospital under the BabySeq protocol,[48] in which newborns are randomized to standard family history collection and care vs full-genome sequencing at birth, with the option of full disclosure to the parents. This “brave new world” approach will not only identify unsuspected syndromes in children, but will also find unsuspected syndromes in their parents, and will identify predispositions to disease expected much later in life—opening the door to early intervention and lifestyle modification. However, it is important to also recognize that, while some may appreciate the benefits of identifying such mutations, syndromes, and predispositions, other patients may live in constant fear of what has been projected—and that particular outcome may never become a reality. Regardless, inexpensive full-genome sequencing is just around the corner and may rapidly make our arguments and concerns moot.

More Need for CDS

The increase in knowledge is continuous and overwhelming, and the human brain is approaching its limit. In genetics specifically, the amount of information is exploding. A query to AuthorMapper[49] regarding articles in Medline that discuss BRCA1 shows 9 articles in the year 1994, when the gene was cloned; that number has grown exponentially—to more than 1,728 in 2015. The National Center for Biotechnology Information Genetic Testing Registry[50] boasts that it has registered more than 32,000 tests for 5,800 conditions and 3,900 genes. It is obvious that we cannot keep up with all the information on just BRCA1, much less for all of breast cancer genetics or for cancer genetics in general—and yet we continue to practice “memory-based medicine.”[51]

To potentially address this challenge, computerized CDS could be investigated as a solution in genetics.[52] CDS accepts machine-readable data about individual patients and then uses computerized knowledge bases, algorithms, guidelines, and models to determine a diagnosis and/or the best management strategy. It then presents that information to the provider in an intuitive format or visualization that helps the provider proceed down the correct path. CDS may help answer the following, as well as many additional questions:

• Who should have genetic testing?

• Which test or panel should be ordered?

• How should the results be interpreted?

• Is a particular variant deleterious?

• What is the risk of cancer(s) for a given gene?

• How can we best screen for or prevent a given cancer?

• How can we best treat a given cancer?

• How should older genetic interpretations be updated as new information becomes available?

Unfortunately, electronic health records (EHRs) lag behind in the tools they provide for CDS, especially as it relates to genetics. Most EHRs store genetic testing results as images of documents. These images cannot be used for CDS, cannot be searched, and cannot be aggregated for research or patient care. It is essential that EHRs adapt quickly to storing structured data and using CDS for genetics.

Summary

Genetic testing has entered a new era and our older paradigms are no longer sufficient. It is critical to find every mutation carrier for every hereditary syndrome before the disease occurs, and to change management of affected individuals in a way that prevents disease or finds it at an earlier, more treatable stage. Whether we achieve this with memory-based medicine, CDS, or population-based testing, we must find a way to accomplish this now.

Acknowledgment: The authors wish to acknowledge Ann S. Adams for her writing and editorial consultation.

Financial Disclosure: Dr. Hughes receives honoraria from Myriad Genetics and Veritas Genetics, and is a founder of and has a financial interest in Hughes Risk Apps, LLC. Dr. Hughes’s interests were reviewed and are managed by Massachusetts General Hospital and Partners HealthCare in accordance with their conflict of interest policies. Dr. Thakuria is a cofounder and Chief Medical Officer of Veritas Genetics. Dr. Plichta and Ms. Griffin have no significant financial interest in or other relationship with the manufacturer of any product or provider of any service mentioned in this article.

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