Coordinator's Message: Reflections

Catherine M. Belt, RN, MSN, AOCN®
Philadelphia, PA
cathy.belt@uphs.upenn.edu
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Catherine M. Belt

Transitions in life are a good time to reflect on where you are, where you have been, and where you are headed. As you read this newsletter, the CAG SIG leadership is changing hands, and we are welcoming our colleague Julie Eggert, PhD, GNP-BC, AGN-BC, AOCN®, FAAN, as SIG Coordinator. Julie brings considerable knowledge and experience from past ONS leadership positions. This is a time of flux for the SIGs as ONS continues its evolution and reorganization. SIGs will have a greater emphasis on electronic communications, and we must translate SIG roles into ONS Communities. Julie will need your support and contributions as the future of these Communities is defined.

In 2013 when I became CAG SIG coordinator-elect, I was filled with trepidation. It was the first national leadership position I had ever held, and I was worried I wasn’t prepared for the journey ahead. I couldn’t have predicted the road I’ve traveled over these past three years. Attending the annual ONS SIG Leadership Weekend has been an invaluable learning opportunity. It is a chance to network with other SIG leaders and meet our hardworking ONS representatives and national staff. Knowing we share the same concerns and commitment to making a difference is comforting. As ONS moves into the future, this dynamic group of leaders is working hard on behalf of their nursing constituents to ensure that the best of the SIG programs is not lost in the transition.

The success of any leader is dependent on his or her supporting cast. I am blessed with a SIG leadership team that is tireless in collaborating and contributing to the continued success of the CAG SIG’s goals. I appreciate their willingness to participate in team conference calls, provide suggestions and feedback, support the biannual newsletter, and commit to a continued focus on cancer genetics nursing. We covered a lot of territory in the past two years. We revised the ONS position statement, “Oncology Nursing: Application of Cancer Genetics and Genomics Throughout the Oncology Care Continuum,” annually to incorporate the rapidly changing fields of cancer risk assessment, genomics, and the role of oncology nursing. Our team contributed to our colleagues’ learning needs through presentations at ONS Congresses and other national nursing forums. Our 2015 SIG meeting was attended by more than 100 nurses, the best turnout we have had in several years. Three of our topic submissions were accepted as podium presentations at the ONS 41st Annual Congress, and this year’s SIG meeting featured an exceptional presentation by Amy Strauss Tranin, APRN, MS, AOCN®, RN-BC.

Many of our SIG members also are members of the International Society of Nurses in Genetics (ISONG), and several of our SIG leaders hold ISONG leadership roles. This interprofessional collaboration has been instrumental in advancing the quest for professional credentialing, particularly the ISONG partnership with the American Nurses Credentialing Center to reintroduce the Advanced Nurse in Genetics certification. We have not abandoned the hope of achieving ONCC credentialing for the cancer genetic nursing specialty. This is unfinished business for future leaders. Our SIG was involved in connecting Jackson Laboratories (JAX) and ONS to submit a grant proposal for a cancer genetics and genomics nursing education program. Working through this process was another learning experience. Although the JAX grant was not funded this year, the company is prepared to work with our leadership team and resubmit the proposal.

The conclusion of my term as SIG coordinator came more quickly than I expected. It has been an incredibly positive learning experience, and I encourage you to take the leap and volunteer to work with the leadership team. I am looking forward to the closure of a nursing career that spanned 43 years and witnessed more evolutions in health care and nursing than I can enumerate. As I look forward to retirement, I am deeply appreciative of this opportunity to contribute to an organization and a nursing specialty that I cherished for the past 33 years. I wish continued success to the CAG SIG.

Introductions

Julie Eggert, PhD, GNP-BC, AGN-BC, AOCN®, FAAN
Greer, SC
jaegger@clemson.edu
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Julie Eggert

This note is to introduce myself as the new coordinator of the CAG SIG, which began at the conclusion of Congress this May. As the newly elected coordinator, I am honored and intimidated to follow in the footsteps of many esteemed colleagues. We have seen many changes over the years, and based on the “Big Change” theme of this Congress, we can anticipate many more. Change can be positive, and I hope you will join me in approaching these next years with a “change can be great” attitude. I pledge to continue the work of our SIG, promoting the understanding of cancer genetics for individuals with inherited cancers and increasing our knowledge of genetic information to target therapies for hereditary mutations. The future is now. It is exciting, and I look forward to working together as these changes offer new opportunities for our patients.

Julie Eggert is the coordinator of the Healthcare Genetics doctoral program at Clemson University in South Carolina. She is a past secretary of the ONS Board of Directors and has more than six years of experience working with clients in a high-risk hereditary cancer clinic. We welcome Julie in her new role as CAG SIG coordinator.

Expanding Genomic Knowledge: Developing Education to Meet Clinicians’ Needs

Kate Reed, MPH, ScM, CGC
Bar Harbor, ME
kate.reed@jax.org
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Kate Reed

Key Points

  • The Clinical and Continuing Education Program (CCEP) at the Jackson Laboratory, a nonprofit organization, is developing educational resources for nurses and other healthcare providers on genomics.
  • CCEP works collaboratively with organizations to develop programs that address specific clinician needs.

Free Resources

Genomics has long played an important role in oncology care, from family history risk assessments, to identifying individuals with a high risk of developing a syndrome, to genomic testing for diagnosis, prognosis, and therapy. The recent explosion of genetic and genomic tests is a result of rapid advances in technology and bioinformatics. Today, if a clinician wants to order a gene panel that includes the BRCA1 and BRCA2 genes to determine hereditary cancer risk, he or she can choose from 150 different panels offered by 26 laboratories (National Center for Biotechnology Information, 2016). In addition, oncologists can order tumor sequencing, which assesses not just one or two but hundreds of potentially targetable variants (Hollebecque, Massard, & Soria, 2014).

To keep up with this rapidly changing landscape, nurses must have an understanding of underlying principles such as genomic variation as well as up-to-date information about the implications of specific variants on cancer risk or treatment efficacy. Nurses are on the front line, explaining these challenging concepts to patients in a way that helps them make informed decisions. To help nurses and other healthcare providers keep up with an evolving knowledge base and integrate that knowledge into clinical care, the Jackson Laboratory (JAX), a nonprofit organization focused on mammalian and human genomics research, is developing a wide range of education resources. These materials range from case-based web modules to skill-building workshops for individuals, hospitals, and training programs. We want to fill education gaps through collaboration, not reinvent the wheel by replicating the great resources currently available.

Although education for students and researchers has long been an integral part of JAX’s mission, clinical education is a comparatively recent focus. Including clinicians reflects JAX’s mission “to discover precise genomic solutions for disease and empower the global biomedical community in the shared quest to improve human health” (JAX, n.d.). The JAX Clinical and Continuing Education Program (CCEP) began in 2013 with the transition of three core staff members and an existing educational portfolio from the National Coalition for Health Professional Education in Genetics (NCHPEG). NCHPEG is an organization founded by the American Medical Association, American Nurses Association, and National Human Genome Research Institute in 1996 to educate clinical providers about how to use the genomic information coming out of the Human Genome Project. CCEP continues to develop genomic education programs in the collaborative spirit embraced by NCHPEG.

In a little more than two years, CCEP developed online modules, eBooks on genomic technologies, and an in-person workshop focused on hereditary cancer in addition to presenting to clinicians in a variety of settings. The interactive, free online modules address family history-based risk assessments, genetic testing, and the integration of genetic information into patient management. The eBooks are both on genomic technologies. Genetic Testing Methods focuses on the testing techniques used clinically, and Genomic Technologies for the Oncology Researcher provides information and videos about the benefits and limitations of technologies being used in clinical research settings.

The workshop, Cancer Genetics Management in the Primary Care Practice, incorporates a standardized patient-provider interaction, audience response, and small group discussions. It was developed in collaboration with the American Society of Human Genetics. After two successful workshops, one in Connecticut and one in Michigan, CCEP worked with the Connecticut Department of Public Health and the Connecticut Nurses Association to implement the workshop in two parts (six hours total) for nurses at the JAX facility in Farmington, CT, this spring. We look forward to working with other partners to hold more workshops in the future.

In addition to these programs, CCEP is collaborating with ONS and other professional organizations to identify educational needs and develop programs to fill those gaps. CCEP hopes to leverage its existing expertise to create programs and materials that will facilitate the development of a knowledgeable workforce that is confident in its ability to integrate genomics appropriately in practice. CCEP welcomes any SIG member interested in education to contact them with thoughts and ideas.

References

Hollebecque, A., Massard, C., & Soria, J.C. (2014). Implementing precision medicine initiatives in the clinic: A new paradigm in drug development. Current Opinion in Oncology, 26, 340-346. doi:10.1097/CCO.0000000000000077

Jackson Laboratory. (n.d.). Mission. Retrieved from https://www.jax.org/about-us/mission

National Center for Biotechnology Information. (2016). Breast cancer diagnostic genetic tests. Genetic Testing Registry. Retrieved from http://www.ncbi.nlm.nih.gov/gtr/all/?term=Breast+cancer+diagnostic+genetic+tests

Evolution of Panel Testing for Hereditary Cancers

Karen Heller, MS, CGC
Dallas, TX
kheller@myriad.com

Edith Smith, DNP, WHNP-BC, AGN-BC
Beverly Hills, CA
edsmith@myriad.com
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Karen Heller
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Edith Smith

Key Points

  • With the advent of panel testing, a more complete genetic evaluation can be performed at once, often at a similar cost to testing for a single syndrome.
  • Next-generation sequencing, also referred to as massively parallel sequencing, involves thousands to millions of simultaneous polymerase chain reactions sequencing numerous small fragments from multiple genes. This is followed by an alignment of all short DNA segments to establish the full sequence through a digital readout.
  • Multigene panel testing is likely to change clinical management for substantially more patients.
  • As technology and science continue to advance, we can expect more opportunities to personalize care for patients and families in a cost-effective, time-efficient manner.

The past few years have seen tremendous growth in the use of multigene panel tests to evaluate patients at risk for hereditary cancer syndromes. This paradigm shift in clinical practice occurred for a number of reasons. Studies demonstrating improved outcomes (Domchek et al., 2010; Jarvinen et al., 2009; Moyer, 2014) confirm the importance of identifying individuals at an increased risk for cancer and offering risk reduction and intensive surveillance options. Increased knowledge about the genetic causes of cancer and the elucidation of concepts such as DNA repair pathways resulted in a greater understanding of the multiple genes that contribute to cancer risk. Technological advances enable laboratories to test multiple genes simultaneously with more efficiency than single-gene testing. Practically speaking, when a number of syndromes and potential genetic causes are on the list of differential diagnoses, it is time and cost prohibitive to test them individually. With the advent of panel testing, a more complete evaluation can be performed at a similar cost as genetic testing for a single hereditary syndrome. Because multiple genes contribute to cancer risk and there is significant overlap in the presentation of several hereditary cancer syndromes, a patient’s personal and family history often is compatible with several possible syndromes. Moreover, patients may not report a history that indicates a particular syndrome because of factors such as small family size, incomplete and age-related penetrance, and lack of family cohesiveness. Panel testing is particularly helpful in cancer genetics because it ensures a more complete assessment for syndromes associated with an overlapping pattern of cancers.

Saam et al. (2015) demonstrated a substantial phenotypic overlap between the two most common hereditary cancer syndromes, hereditary breast and ovarian cancer syndrome (HBOC) and Lynch syndrome (LS or hereditary nonpolyposis colorectal cancer syndrome). They found that 7% of patients tested for HBOC also met testing criteria for LS, and almost 30% of patients tested for LS also met testing criteria for HBOC (Saam et al., 2015). As new data are published, professional societies such as the National Comprehensive Cancer Network (NCCN) provide updated management guidelines for additional gene mutations. For example, recent NCCN Guidelines® added recommendations for breast magnetic resonance imaging screening for carriers of PALB2, CHEK2, ATM, or CDH1 mutations and risk-reducing salpingo-oophorectomy for carriers of BRIP1, RAD51C, or RAD51D mutations based on current evidence of associated cancer risks (NCCN, 2016).

Historically, the gold standard for genetic testing was gene sequencing using the Sanger method, which involves sequencing all exons in a single gene with separate polymerase chain reactions (PCRs). Next-generation sequencing (NGS), also referred to as massively parallel sequencing, involves thousands to millions of simultaneous PCRs sequencing numerous small fragments of multiple genes. This is followed by an alignment of all short DNA segments, establishing the full sequence through a digital readout. This improved efficiency translates into a less expensive method of sequencing. However, clinically significant variants (mutations) must be found within massive amounts of data, and assays must be optimized to ensure that each and every relevant base pair is read accurately. The term “depth of coverage” refers to the number of times any particular base pair is read.

To demonstrate the equivalent accuracy of an NGS test compared to Sanger sequencing, a head-to-head validation study as performed by Judkins et al. (2015) is necessary. Although the cost of sequencing base pairs is cheaper with NGS, more genes sequenced lead to more genetic variants detected, and additional laboratory investments must be made for accurate variant interpretation. Recent literature highlights inconsistencies in variant classifications among testing labs (Thompson et al., 2014; Vail et al., 2015). This is a concern for providers because recommended medical management is frequently determined by genetic test results. To address laboratory inconsistencies and the potential for patient harm, the U.S. Food and Drug Administration stated its intention to regulate laboratory developed tests (U.S. Department of Health and Human Services, 2014).When a panel approach is used for hereditary cancer testing, more high-risk patients are identified compared to testing for a single syndrome.

When a panel approach is used for hereditary cancer testing, more high-risk patients are identified compared to testing for a single syndrome. In a study of patients with breast cancer referred for BRCA1 and BRCA2 mutation testing, Tung et al. (2015) found a 9% positive mutation detection rate in BRCA1 and BRCA2, but a 14% positive mutation detection rate when patients were tested with a 25-gene panel (Tung et al., 2015). In a study of patients with suspected LS, Yurgelun et al. (2015) identified 9% with LS mutations, but 15% tested positive for gene mutations using an expanded 25-gene panel.

When positive results are found in genes with established medical management guidelines, there is potential to improve clinical management. Desmond et al. (2015) reported that multigene panel testing yielded findings likely to change the clinical management for substantially more patients than BRCA1 and BRCA2 testing alone. An interim analysis of 332 patients tested with a multigene panel suggested no increase in distress with 81% of patients wanting all of their genetic test results and 87% expressing no regrets when learning their results (Kurian et al., 2015).

Since 2014, the NCCN Guideline for Hereditary Breast and Ovarian Cancer testing algorithm includes the option of first-line testing using a multigene panel as an alternative to testing for BRCA1 and BRCA2 mutations alone (NCCN, 2016). With the widespread provider use of panel testing for hereditary cancer and the inclusion of panel testing in the NCCN Guidelines, multigene panel tests are being evaluated for inclusion in coverage policies (Balliet, 2015).

It is an exciting time in cancer genetics and oncology nursing. Tremendous advancements have been made in technology and the detection and interpretation of genetic variants, improving the identification of at-risk patients and tailoring treatment options for those already affected. As technology and science continue to advance, we can expect more opportunities to personalize care for patients and their families in a cost-effective, time-efficient manner.

References

Balliet, R. (2015). Hayes, Inc. unveils multigene panel testing white paper. Retrieved from http://www.hayesinc.com/hayes/media_center/press-releases/hayes-inc-unveils-multigene-panel-testing-white-paper/

Desmond, A., Kurian, A.W., Gabree, M., Mills, M.A., Anderson, M.J., Kobayashi, Y., . . . Ellisen, L.W. (2015). Clinical actionability of multigene panel testing for hereditary breast and ovarian cancer risk assessment. JAMA Oncology, 1, 943-951. Retrieved from http://oncology.jamanetwork.com/article.aspx?articleid=2425836

Domchek, S.M., Friebel, T.M., Singer, C.F., Evans, D.G., Lynch, H.T., Isaacs, C., . . . Rebbeck, T.R. (2010). Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality. JAMA, 304, 967-975. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2948529/

Jarvinen, H.J., Renkonen-Sinisalo, L., Aktan-Collan, K., Peltomaki, P., Aaltonen, L.A., & Mecklin, J. (2009). Ten years after mutation testing for Lynch syndrome: Cancer incidence and outcome in mutation-positive and mutation-negative family members. Journal of Clinical Oncology, 27, 4793-4797. Retrieved from http://jco.ascopubs.org/content/27/28/4793.long

Judkins, T., Leclair, B., Bowles, K., Gutin, N., Trost, J., McCulloch, J., . . . Timms, K. (2015). Development and analytic validation of a 25-gene next generation sequencing panel that includes the BRCA1 and BRCA2 genes to assess hereditary cancer risk. BMC Cancer, 15, 215. doi:10.1186/s12885-015-1224-y

Kurian, A.W., Idos, G., McDonnell, K., Ricker, C., Sturgeon, D., Culver, J., . . . Gruber, S.B. (2015). The patient experience in a prospective trial of multiplex gene panel testing for cancer risk [Poster presented at the San Antonio Breast Cancer Symposium, TX]. Retrieved from https://www.sabcs.org/Program/Poster-Sessions/Poster-Session-2

Moyer, V.A. (2014). Risk assessment, genetic counseling, and genetic testing for BRCA-related cancer in women: U.S. Preventive Services Task Force Recommendation Statement. Annals of Internal Medicine, 160, 271-281. Retrieved from http://annals.org/article.aspx?articleid=1791499

National Comprehensive Cancer Network. (2016). NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®): Genetic/familial high-risk assessment: Breast and ovarian [v.1.2016]. Retrieved from http://www.nccn.org/professionals/physician_gls/pdf/genetics_screening.pdf

Saam, J., Arnell, C., Theisen, A., Moyes, K., Marino, I., Roundy, K.M., & Wenstrup, R.J. (2015). Patients tested at a laboratory for hereditary cancer syndromes show an overlap for multiple syndromes in their personal and familial cancer histories. Oncology, 89, 288-293. doi:10.1159/000437307

Thompson, B.A., Spurdle, A.B., Plazzer, J., Greenblatt, M.S., Akagi, K., Al-Mulla, F., . . . Genuardi, M. (2014). Application of a 5-tiered scheme for standardized classification of 2,360 unique mismatch repair gene variants in the InSiGHT locus-specific database. Nature Genetics, 46, 107-117. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4294709/

Tung, N., Battelli, C., Allen, B., Kaldate, R., Bhatnagar, S., Bowles, K., . . . Hartman, A. (2015). Frequency of mutations in individuals with breast cancer referred for BRCA1 and BRCA2 testing using next-generation sequencing with a 25-gene panel. Cancer, 121, 25-33. Retrieved from http://onlinelibrary.wiley.com/doi/10.1002/cncr.29010/full

U.S. Department of Health and Human Services. (2014). FDA takes steps to help ensure the reliability of certain diagnostic tests. U.S. Food and Drug Administration news release. Retrieved from http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm407321.htm

Vail, P.J., Morris, B., van Kan, A., Burdett, B.C., Moyes, K., Theisen, A., . . . Eggington, J.M. (2015). Comparison of locus-specific databases for BRCA1 and BRCA2 variants reveals disparity in variant classification within and among databases. Journal of Community Genetics, 6, 351-359. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/pmid/25782689/

Yurgelun, M.B., Allen, B., Kaldate, R.R., Bowles, K.R., Judkins, T., Kaushik, P., . . . Syngal, S. (2015). Identification of a variety of mutations in cancer predisposition genes in patients with suspected Lynch syndrome. Gastroenterology, 149, 604-613. Retrieved from http://www.gastrojournal.org/article/S0016-5085(15)00678-2/fulltext

Precision Medicine: Somatic Genomic Tumor Testing

Amy Strauss Tranin, APRN, MS, AOCN®, RN-BC
Leawood, KS
amy.tranin@nanthealth.com
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Amy Strauss Tranin

Have you ever heard of a terabyte? One terabyte is equal to one trillion bytes, which is the amount of data generated from the whole-genome (DNA) and whole-transcriptome (RNA) sequencing of a tumor tissue sample and blood from one patient. To put it another way, one terabyte is equal to five 53 ft tractor-trailer trucks filled with 140 kb Apple Disk II floppies (remember those?). Just 10 years ago, the thought that the entire genomic sequence of a person’s tumor, embedded in a paraffin block no less, could be compared to their own blood in a reasonable amount of time to make treatment decisions would have seemed like science fiction. The need for a terabyte of storage for each person also would have seemed unfathomable.

The Human Genome Project opened the way for the comprehensive sequencing efforts of human cancers, revealing the genomic landscapes of the most common. Cancer is a disease of the genome, caused by many types of alterations, including single nucleotide variants, insertions, deletions, amplifications, and rearrangements (Kandoth et al., 2013). These genomic changes have clinical implications in the prognosis, diagnosis, and selection of therapies. Most tumors contain a small number of driver alterations, typically two to eight alterations per tumor, which provide a selective survival and growth advantage for tumors but also can serve as a fingerprint for the immune system to identify. Tumors possess a larger number of passenger alterations, which offer no survival or growth advantage. Driver genes can be classified into 12 signaling pathways that regulate three core cellular processes, cell death, cell survival, and genome maintenance (Vogelstein et al., 2013).

The rate of chromosomal changes in cancer is increased (Vogelstein et al., 2013). Most tumors exhibit aneuploidy, or widespread changes in chromosome numbers. Other chromosomal changes are inversions and translocations. Tumors have dozens of translocations. However, most are passenger alterations rather than driver alterations. Translocations generally fuse two genes that typically are not next to each other to create an oncogene such as the BCR-ABL mutation seen in chronic myelogenous leukemia. In a small number of cases, the resulting fusion can inactivate a tumor-suppressor gene by truncating it or separating it from its promoter.

Although different from the rate of chromosomal changes, the rate of point mutations in tumors is similar to that of normal cells (Vogelstein et al., 2013). Additional genetic changes commonly found in tumors are gene deletions and amplifications. Homozygous deletions often involve one or a few genes, and the target is always a tumor-suppressor gene. Gene amplifications result in protein products that are expressed in abnormally high quantities. Amplifications, for example, HER2, potentiate the activity of the downstream protein effector simply because the tumor cell contains 10-100 copies of the gene per cell compared to the two copies present in normal cells. Despite intensive efforts, consistent genetic alterations distinguishing metastasizing cancers from cancers that have not yet metastasized remain to be identified (Vogelstein et al., 2013).

Somatic genetic testing can take many forms including cytogenetics, fluorescence in situ hybridization, arrays, single-gene mutation testing, panel gene testing, and whole-exome, whole-genome, or whole-transcriptome sequencing. Next-generation sequencing output can include filtered sequencing files or annotated variant files. These variant files must be classified using online databases, published literature, and internal data. This can vary between laboratories (Vandeweyer, Van Laer, Loeys, Vanden Bulcke, & Kooy, 2014).

Targeted sequencing, also called hotspot or panel testing, is highly sensitive but can miss key alterations. The most comprehensive somatic tumor testing includes whole-genome (DNA coding and noncoding regions), whole-exome (DNA coding), and whole-transcriptome (RNA) sequencing. These give the most complete picture of a patient’s genomic profile. Regardless of test type, an annotated genome report of relevant clinical findings is the clinical test outcome. The report provides insight into tumor alterations, which can direct treatment decisions for on- and off-label agents and determine a patient’s eligibility for clinical trials. Any secondary (i.e., incidental) nontumor germline findings (if a control blood sample is sequenced) also are reported to the ordering physician for confirmation with commercially available germline testing.

Nurses working in genetics and genomics will be called on to help health professionals and patients understand somatic genomic test results. There often is confusion about somatic testing, especially when it involves normal blood as a comparator and incidental findings are included in the report. Nurses in genetics and genomics should understand the strengths and weaknesses of somatic tumor testing methodologies and the laboratories in which they are performed to assist in interpreting results. Somatic tumor testing is an emerging science. Nurses must be active in the research processes and share their knowledge and experience in specialty organizations such as the ONS Cancer Genetics SIG.

References

Kandoth, C., McLellan, M.D., Vandin, F., Ye, K., Niu, B., Lu, C.,. Ding, L. (2013). Mutational landscape and significance across 12 major cancer types. Nature, 502, 333–339. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3927368/

Vandeweyer, G., VanLaer, L., Loeys, B., Vanden Bulcke, T., & Kooy, R.F. (2014). VariantDB: A flexible annotation and filtering portal for next generation sequencing data. Genome Medicine, 6, 74-84. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4210545/

Vogelstein, B., Papadopoulos, N., Velculescu, V.E., Zhou, S., Diaz, L.A., & Kinzler, K.W. (2013). Cancer genome landscapes. Science, 339, 1546-1558. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3749880/

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