Patient DOI 10.1007/s40271-014-0089-5
CURRENT OPINION
Walking in the Shoes of Patients, Not Just in Their Genes: A Patient-Centered Approach to Genomic Medicine Neeraj K. Arora • Bradford W. Hesse Steven B. Clauser
•
Ó Springer International Publishing Switzerland (outside the USA) 2014
Abstract Genomic technologies are increasing the precision with which clinicians can assess an individual patient’s risk for developing diseases and identify which patients are likely to benefit from specific treatments. Also advocating for a shift away from a one-size-fits-all approach is the growing emphasis on ‘‘patient-centered’’ care. Using examples from breast cancer, we make a case for why, in order to optimize patient health outcomes, genomic medicine will need to be practiced within a patient-centered framework. We present a six-function conceptual framework for patient-centered care and discuss findings from a national survey evaluating the patientcenteredness of care delivered in the USA.
Key Points for Decision Makers In order to maximize the potential of the genomic revolution in healthcare delivery, genomic medicine needs to be practiced within a patient-centered framework that takes a whole-person approach rather than focusing only on the person’s genes. A six-function conceptual framework for optimizing the patient-centeredness of care has been developed by the National Cancer Institute. National survey data of the American public reveal important deficits in the delivery of patient-centered care on each of the six key functions of patientcenteredness.
1 Introduction
N. K. Arora (&) Division of Cancer Control and Population Sciences, National Cancer Institute, NIH, 9609 Medical Center Drive, 3E514, MSC 9762, Bethesda, MD 20892-9762, USA e-mail: [email protected] B. W. Hesse Division of Cancer Control and Population Sciences, National Cancer Institute, NIH, Bethesda, MD, USA S. B. Clauser Patient-Centered Outcomes Research Institute, Washington, DC, USA
Genomic technologies are increasing the precision with which clinicians can assess patients’ risk for developing diseases and identify which patients are likely to benefit from specific treatments [1]. This new paradigm aims to deliver the right medical interventions to the right patient at the right time [2, 3]. Also advocating for a shift away from a one-size-fits-all approach is the growing emphasis on ‘‘patient-centered’’ care (PCC) [4, 5]. The Institute of Medicine (IOM) defines patient-centeredness as ‘‘providing care that is respectful of and responsive to individual patient preferences, needs, and values, and ensuring that patient values guide all clinical decisions’’ [6, p6]. In order to optimize patient health outcomes, these two paradigms of genomic medicine and PCC will need to be integrated
N. K. Arora et al.
with each other. In this commentary, we present a conceptual framework for facilitating PCC, discuss findings from a recent national survey on the state of patient-centeredness of healthcare in the USA, and, using examples from breast cancer, highlight the salience of facilitating patient-centered aspects of care in a healthcare environment increasingly informed by genomic medicine.
5.
2 Functions of Patient-Centered Care In order to understand the key functions of PCC that will need to be supported by healthcare systems to delivery high-quality care, the National Cancer Institute (NCI) commissioned a thorough review and synthesis of the scientific literature. In their report, authors Epstein and Street [7] outlined a conceptual framework for PCC composed of six critical functions. To stimulate future research, this report also discussed various pathways and mechanisms by which the six PCC functions are likely to impact patient health outcomes [7, 8]. 1.
2.
3.
4.
Fostering healing relationships: In addition to wanting evidence-based medical treatments that are likely to maximize their chances of positive clinical outcomes, patients seek care from clinicians who they can trust and rely on to address their health needs. Clinicians who take the time to know their patient as a person and understand how their illness impacts their daily life are more likely to foster long-term trust. Similarly, healthcare systems that move from a fragmented, ‘‘transaction-focused’’ model of care to a continuous, ‘‘relationship-focused’’ model engender greater patient loyalty while augmenting the value of care provided in service of the ‘‘whole patient’’ [9, 10]. Exchanging information: Patients need support from clinicians to make sense of complex medical information that they may obtain from multiple sources. Healthcare systems need to provide medical information in a manner that is easily understood and retained by patients. They also need to inculcate active listening skills to help patients feel comfortable in disclosing personal information that may be important for decision making. Facilitating decision making: While a trusting relationship and information exchange are important for decision making, to facilitate informed decision making, clinicians also need to support patients in their own decisional deliberations by helping them think through their values and preferences as they jointly evaluate various medical options. Responding to emotions: Being at a high risk for, or living with, a potentially life-threatening and/or long-
6.
term chronic illness can result in significant patient distress. To enhance patients’ emotional well-being, clinicians need to reliably assess patients’ distress, legitimize their feelings, show empathy, and where possible provide patients with tangible help to address their negative emotions. Enabling self-management: Given that a large majority of patient care takes place outside the healthcare setting, patients need support from the healthcare system in preparing them for taking care of their health in between visits. This includes support for care coordination, managing symptoms and side effects, engaging in healthy lifestyles, and ensuring adherence to treatments. Managing uncertainty: Patients experience a range of illness-related uncertainties that are scientific, personal, or practical in nature and can significantly impact their well-being [11]. Clinicians need to be aware of patients’ feelings of uncertainty and manage them by facilitating the other five functions of PCC.
3 Walking in the Shoes of Patients To evaluate the state of ‘‘patient-centeredness’’ from the perspective of patients in the general US population, we developed, tested, and included six questions addressing the six PCC functions for administration in the NCI’s Health Information National Trends Survey (HINTS 4, cycle 1). The HINTS program was launched by the NCI in 2001 as a means for assessing the diffusion of health communication messages and strategies at a time of extraordinary change in the overall health information environment [12]. The original program was designed to administer computer-assisted telephone interviews biennially through a list-assisted, random-digit-dial survey of non-institutionalized adults in the USA over 18 years of age. Because of falling response rates among telephone surveys and the increased pace of change in communication technology, the NCI reengineered the survey to be administered by paper and pencil using a randomly drawn sample of addresses from a list of US postal addresses and to be administered over a series of four cycles over a 3-year period [13, 14]. The first cycle of the newly reengineered survey was in the field from October 25, 2011 to February 7, 2012; data from this survey are discussed below. A series of 50 replicate weights were generated to account for the complex survey design and to adjust prevalence estimates based on post-stratification adjustments from census data. The PCC questions asked respondents to report their experiences of how often in the past 12 months their providers addressed each of the six PCC functions
Walking in the Shoes of Patients
(N = 3,322; see Fig. 1 for exact item wording). As shown in Fig. 1, a large proportion of the American population reported that they ‘‘always’’ received PCC (45–61 % across the six functions). However, several deficiencies were reported. Our data show that one out of every four Americans (23 %) who received healthcare in the USA reported that their healthcare providers rarely (never or sometimes) paid attention to their emotions, almost one in five (18 %) were rarely involved in decision making as much as they wanted, and one in four rarely received help in dealing with feelings of uncertainty about their health or healthcare. Our data also suggest that at least one in ten Americans are unable to ask all of their health-related questions during medical visits, they rarely understand the things they need to do to take care of their health once they leave the doctor’s office, and they feel they cannot rely on the healthcare system to take care of their healthcare needs. We contend that in a highquality healthcare delivery system, we should be 95 % confident that patients will receive PCC most of the time, if not all the time (usually or always). Thus, the error rate in delivering sub-optimal PCC should be no more than 5 % compared with the current levels of 11–26 % (i.e., those who had a response of never or sometimes across the six patient-centered functions in our survey). Similar findings highlighting room for improvement in delivering PCC have been reported recently by the IOM [15].
4 Patients’ Care Experiences and Genomic Medicine While our national data suggest the need to optimize the six PCC functions in general, the impetus for doing so is especially high when we consider applications of genomics in clinical practice. To illustrate how the six-function framework may serve to support patient-centeredness in an environment enabled by genomic medicine, we consider two common applications of genomics related to germline genomic testing for breast cancer disease risk prediction and somatic genomic testing for predicting risk of breast cancer recurrence and individualizing chemotherapy treatment decisions [16]. 4.1 Disease Risk Prediction Approximately 5–10 % of all breast cancers have a genetic component associated with them [17]. The most common cause of hereditary breast cancer is a mutation in either the BRCA1 or BRCA2 gene. A BRCA1 or BRCA2 mutation results in a substantial increase in lifetime risk of breast cancer from 12 % for the average woman to 50–60 % for those with a mutation [18]. Interest in BRCA testing has soared significantly since 2013, after actress and director Angelina Jolie reported in the New York Times that she had the BRCA1 mutation and underwent preventive double mastectomy to reduce her risk of dying from breast cancer [19, 20]. Primary care providers and genetics specialists reported what has been termed ‘‘the Angelina Jolie effect,’’
70 61
60
Weighted Percentage
60
54
52
50
45 41
40 32
30 20
26
33
33 30
29 26
23 18
14
13
11
10 0
Informaon
Emoons
Decisions
Self Mgt
Uncertainty Relaonships
Funcons of Paent-Centered Care (PCC)* Never/Somemes
Fig. 1 Weighted percentage of US adults’ reports on the patientcenteredness of healthcare delivery in the U.S. *Data were collected as part of the National Cancer Institute’s 2012 Health Information National Trends Survey (HINTS4, cycle 1). Responders who saw a healthcare provider in the past 12 months (N = 3,322) were asked to report on their PCC experiences in the past 12 months on a never, sometimes, usually, always scale. The following six PCC questions were asked: 1. Fostering healing relationships: How often did you feel you could rely on your healthcare providers to take care of your healthcare needs? 2. Exchanging information: How often did your
Usually
Always
providers give you the chance to ask all the health-related questions you had? 3. Facilitating decision making: How often did your providers involve you in decisions about your health care as much as you wanted? 4. Responding to emotions: How often did your providers give the attention you needed to your feelings and emotions? 5. Enabling self-management: How often did your providers make sure you understood the things you needed to do to take care of your health? 6. Managing uncertainty: How often did your providers help you deal with feelings of uncertainty about your health or health care?
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a surge in queries from women across the country on whether they should receive BRCA testing and/or undergo bilateral mastectomy [18, 21]. The typical process related to testing for BRCA mutations in many comprehensive cancer centers that have dedicated clinical genetics clinics may involve two face-toface meetings with the patient, first to assess the appropriateness of BRCA testing by conducting a comprehensive assessment of family cancer history followed by a consultation with a trained genetic counselor for those women for whom BRCA testing may be appropriate [22]. To derive maximum benefit from BRCA testing on short- and longterm patient outcomes, clinical teams interacting with patients and family members will have to provide them with ongoing support addressing several needs related to PCC during these initial visits and beyond. For example, women without a personal history of breast cancer who test positive for BRCA1 or BRCA2 mutation face several complex choices for early detection and/or risk reduction. These include yearly screening with mammography and breast magnetic resonance imaging (MRI), chemoprevention with tamoxifen, and surgical options, including prophylactic mastectomy [18, 22–24]. Each of these approaches has its own downsides. Annual cancer screening can result in significant psychological distress, especially given false positive results that may be encountered in breast MRI screening. Side effects of surgical and pharmacological interventions include implications for body image, early menopause, fertility and sexual functioning problems, weight gain, and increased risk of cardiovascular disease [18, 22–24]. Unlike the case of women diagnosed with invasive breast cancer, women who test positive for BRCA mutations should not, in most cases, feel a time pressure to make a treatment or surveillance decision within the context of one or two initial medical visits. These women and their family members need coordinated, ongoing support from the multiple providers they are likely to see during this time, including genetic counselors, primary care physicians, and oncology specialists, in weighing the risks and benefits of different approaches and incorporating their values and preferences in decisions that are likely to have significant long-term implications for their life [24]. Moreover, given the several side effects associated with various options, clinical teams will have to recognize and address those physical, emotional, and social functioning problems over time in a way that minimizes decision regret among patients. Women found to carry a BRCA mutation will also need additional counseling and support from their clinical teams to facilitate communication with their family members about the implication of the test results on their family [18]. Population level studies are needed to assess the extent to which women receive ongoing support,
beyond initial genetic counseling consultations, from a coordinated, healthcare system to meet their various medical and psychosocial needs. 4.2 Individualizing Chemotherapy Treatment Nearly 50 % of breast cancers diagnosed in the USA are early-stage, estrogen receptor-positive, lymph node-negative cancers. Many patients with such a diagnosis receive adjuvant chemotherapy and experience debilitating side effects despite limited survival benefits [25]. To improve individualizing of adjuvant treatments, gene expression profiling (GEP) of breast tumors using tests such as the Oncotype DxTM, a 21-gene assay, is being used to identify women who are more likely to benefit from chemotherapy on the basis of their recurrence risk scores (RSs) [26, 27]. A systematic review and meta-analysis of 23 studies on the impact of Oncotype DxTM on clinical practice shows that a little less than half of all patients who take the test receive a low RS, 39 % receive an intermediate RS, and 12 % receive a high RS [25]. In at least one in three cases, the Oncotype DxTM results have been shown to change the clinician’s prior recommendations related to adjuvant chemotherapy. While GEP tests like the Oncotype DxTM hold significant promise to individualize chemotherapy decisions, similar to our observations for germline genomic testing using the example of BRCA mutations, several patient needs related to the six patient-centered functions will have to be systematically addressed to maximize benefit from these tests. A limited number of studies have examined patient experiences with GEP and its impact on their treatment decision making. Bombard et al. [28] reported from their qualitative findings that many women misunderstood the purpose of the test, some reported information overload while receiving the test results, and many considered the GEP test to provide them with the most definitive information to facilitate their chemotherapy decision. Similarly, Tzeng et al. [26] reported a third of their sample lacked a complete understanding of the discussions they had related to GEP and one in four experienced distress related to the test results. The authors suggest there is a great need to aid and improve risk communication and decision making within the context of using GEP for adjuvant chemotherapy decisions. Depending upon the recurrence RS, specific patientcentered issues will need to be addressed. For example, women with high RSs are likely to choose chemotherapy. In addition to knowing their RS, they will need adequate information about expected short- and long-term side effects in a way they can easily understand. Knowledge of a higher probability of recurrence and anticipation of chemotherapy-related side effects can result in significant distress that will need to be addressed by clinical teams. While undergoing chemotherapy, patients will need self-
Walking in the Shoes of Patients
management support to manage their symptoms and side effects at home. While several national efforts have been made to integrate palliative care for patients from the time of diagnosis and there exists a large evidence base for many interventions that clinical teams can use to evaluate and manage a variety of patient symptoms [29, 30], several studies continue to report significant short- and long-term unmet symptom needs experienced by cancer patients and survivors [31–33]. The benefit of chemotherapy for the many patients who receive an intermediate RS is not clear. The clinical uncertainty of the test result needs to be communicated to these women in a manner that minimizes distress. Clinicians will need to support them in thinking through their values and preferences while making the decision about chemotherapy in the face of uncertainty. Interventions grounded in decision analysis that facilitate elicitation and clarification of patient preferences can help optimize patient–clinician communication and enhance patient engagement [28, 34, 35]. For patients who decide against chemotherapy, long-term distress related to fear of recurrence needs to be recognized and addressed. Women with low RSs are unlikely to choose chemotherapy and many consider the GEP test to be their savior rescuing them from experiencing unnecessary side effects [28]. However, these women still need ongoing surveillance to monitor for late effects of other treatments and for secondary malignancies. Clinicians will need to engage them in developing and implementing a survivorship care plan to facilitate such surveillance and promote a healthy lifestyle. Khoury et al. [36] describe four phases of translational genomics that move from basic genomic discoveries to candidate health applications (T1), to assessing the value of the genomic applications for clinical practice leading to development of evidence-based guidelines (T2), to implementing the guidelines in clinical practice (T3), to evaluating the impact of genomic applications on individual and population health outcomes (T4). Bombard et al. [16] note that significant gaps currently exist in the evidence base for genomics applications to successfully move from T1 to T4 and call for more focused research in several areas, including outcomes and health services research. As we have illustrated in the examples above, in order to maximize the impact of genomic applications on patient health outcomes, explicit efforts will need to be made to incorporate the patient’s perspective in genomics translational research as well as in clinical practice. 5 Conclusion As efforts towards implementing the Patient Protection and Affordable Care Act unfold [37], an emphasis on
patient-centeredness is likely to increase in research and practice, as evidenced by the establishment of the PatientCentered Outcomes Research Institute (PCORI) [38] and implementation of innovative models of care such as the patient-centered medical home [39, 40] and accountable care organizations [41, 42]. Even at the policy level, a focus on delivering PCC is being incorporated in payment models. For example, the Centers for Medicare & Medicaid Services’ implementation of a value-based purchasing program proposes to reimburse hospitals in part on their performance on patient-reported, patient-centered measures [43]. At the same time, genomically informed medicine is creating an environment that is awash in a deluge of data. In a report on evidence-based medicine by the IOM, authors recounted the observation that in 1990 a typical clinician or patient would have to bear roughly five to seven individual facts in mind in order to give due diligence to a treatment decision. By 2020, with the burgeoning availability of structural data on haplotypes and single nucleotide polymorphisms, the documentation of gene expression profiles, and a more thorough assessment of proteomic and effector molecules, the number of individual facts to consider for a precision-based treatment decision will likely exceed 1,000 [44]. Clearly, innovation will be needed to package this information and to reengineer clinical care processes so as to not outstrip the capacities of physicians, care teams, genetic counselors, patients, and caregivers [45, 46]. The goal in this new world is to engineer a system that follows the functional requirements of the PCC framework as articulated earlier; that is, to create a system with 95 % effectiveness in meeting patients’ expectations for a healing relationship in which they exchange information effectively, cope with uncertainty, clarify their emotions, make value-congruent decisions, and are effective in self-management. In an era of healthcare reform and genomic medicine, patient health outcomes are likely to be optimized when we take a comprehensive approach from the patient’s genes to the whole patient. In this new paradigm, healthcare systems will need to support clinical teams in their efforts to facilitate the patient-centered aspects of care, for we must not forget the patient in the pursuit of his or her genes. Acknowledgments This article reflects the personal opinions of the authors and does not necessarily represent any official position of the National Cancer Institute, National Institutes of Health, or the PatientCentered Outcomes Research Institute. The authors wish to thank Muin Khoury, MD, PhD for his helpful feedback on an initial draft of the manuscript. Conflict of Interest interest.
None of the authors have any conflict of
N. K. Arora et al. Authors contribution All authors contributed to the conceptualization, writing, and final approval of the manuscript.
References 1. Institute of Medicine. The value of genetic and genomic technologies: workshop summary. Washington, DC: The National Academies Press; 2010. 2. Collins FS, Guttmacher AE. Genetics moves into the medical mainstream. JAMA. 2001;286(18):2322–4. 3. Issa AM. Personalized medicine and the practice of medicine in the 21st century. Mcgill J Med. 2007;10(1):53–7. 4. Epstein RM, Fiscella K, Lesser CS, Stange KC. Why the nation needs a policy push on patient-centered health care. Heath Aff (Millwood). 2010;29:1489–95. 5. Davis K, Schoenbaum SC, Audet AM. A 2020 vision of patientcentered primary care. J Gen Intern Med. 2005;20(10):953–7. 6. Institute of Medicine. Crossing the quality chasm: a new health system for the 21st century. Washington, DC: National Academies Press; 2001. 7. Epstein RM, Street RL, Jr. Patient-centered communication in cancer care: promoting healing and reducing suffering. Bethesda: National Cancer Institute, NIH publication no. 07-6225; 2007. 8. Street RL Jr, Makoul G, Arora NK, Epstein RD. How does communication heal? Pathways linking clinician-patient communication to health outcomes. Patient Edu Couns. 2009;74:295–301. 9. Zuboff S, Maxmin J. The support economy: why corporations are failing individuals and the next episode of capitalism. New York: Viking; 2002. p. 2002. 10. Institute of Medicine. Cancer care for the whole patient: meeting psychosocial health needs. Washington, DC: The National Academies Press; 2008. 11. Han PKJ, Klein WMP, Arora NK. Varieties of uncertainty in healthcare: a conceptual taxonomy. Med Decis Making. 2011;31:828–38. 12. Nelson DE, Rimer BK, Kreps GL, Hesse BW, Viswanath KV, Croyle RT, Willis G, Arora NK, Weinstein N, Alden S. The Health Information National Trends Survey (HINTS): development, design, and dissemination. J Health Commun. 2004;9:1–18. 13. Finney Rutten LJ, Davis T, Beckjord EB, Blake K, Moser RP, Hesse BW. Picking up the pace: changes in method and frame for the Health Information National Trends Survey (2011–2014). J Health Commun. 2012;17:979–89. 14. Rutten LJF, Hesse BW, Moser RP, Kreps GL, editors. Building the Evidence Base in Cancer Communication. Cresskill: Hampton Press; 2011. 15. Novelli WD, Halvorson GC, Santa J. Recognizing an opinion: findings from the IOM evidence communication innovation collaborative. JAMA. 2013;308:1531–2. 16. Bombard Y, Bach PB, Offit K. Translating genomics in cancer care. J Natl Compr Cancer Netw. 2013;11(11):1343–53. 17. Nelson HD, Huffman LH, Fu R, Harris EL. U.S. Preventive Services Task Force. Genetic risk assessment and BRCA mutation testing for breast and ovarian cancer susceptibility: systematic evidence review for the U.S. Preventive Services Task Force. Ann Intern Med. 2005;143(5):362–79. 18. McCarthy AM, Armstrong K. The role of testing for BRCA1 and BRCA2 mutations in cancer prevention. JAMA Intern Med. 2014;174(7):1023–4. 19. Jolie A. My medical choice. The New York Times. http://www. nytimes.com/2013/05/14/opinion/my-medical-choice.html. 14 May 2013.
20. Neporent L. Angelina Jolie’s double mastectomy fueling national debate. http://abcnews.go.com/Health/angelina-jolies-doublemastectomy-fueling-national-debate/story?id=19315336. 4 June 2013. 21. Matloff ET. The Angelina effect: rising interest in genetic testing creates opportunities for patients—and profit. Am J Manag Care. 2014;20(special issue 3):SP67. 22. Connors LM, Voian N, Shi Y, Lally RM, Edge S. Decision making after BRCA genetic testing: down the road of transition. Clin J Oncol Nurs. 2014;18(3):E58–63. 23. Hesse-Biber S. The genetic testing experience of BRCA-positive women: deciding between surveillance and surgery. Qual Health Res. 2014;24(6):773–89. 24. Stan DL, Shuster LT, Wick MJ, Swanson CL, Pruthi S, BakkumGamez JN. Challenging and complex decisions in the management of the BRCA mutation carrier. J Womens Health. 2013;22(10):825–34. 25. Carlson JJ, Roth JA. The impact of the Oncotype Dx breast cancer assay in clinical practice: a systematic review and metaanalysis. Breast Cancer Res Treat. 2013;141(1):13–22. 26. Tzeng JP, Mayer D, Richman AR, et al. Women’s experiences with genomic testing for breast cancer recurrence risk. Cancer. 2010;116:1992–2000. 27. Lo SS, Mumby PB, Norton J, et al. Prospective multicenter study of the impact of the 21-gene recurrence score assay on medical oncologist and patient adjuvant breast cancer treatment selection. J Clin Oncol. 2010;28(10):1671–6. 28. Bombard Y, Rozmovits L, Trudeau ME, Leighl NB, Deal K, Marshall DA. Patients’ perceptions of gene expression profiling in breast cancer treatment decisions. Curr Oncol. 2014;21(2):e203–11. 29. Institute of Medicine. Improving Palliative Care for Cancer: Summary and Recommendations. Washington, DC: The National Academies Press; 2001. 30. Loprinzi CL, Wolf SL, Barton DL, Laack NN. Symptom management in premenopausal patients with breast cancer. Lancet Oncol. 2008;9(10):993–1001. 31. Yoon J, Malin JL, Tisnado DM, Tao ML, Adams JL, Timmer MJ, Ganz PA, Kahn KL. Symptom management after breast cancer treatment: is it influenced by patient characteristics? Breast Cancer Res Treat. 2008;108(1):69–77. 32. Kent EE, Mitchell SA, Oakley-Girvan I, Arora NK. The importance of symptom surveillance during follow-up care of leukemia, bladder, and colorectal cancer survivors. Support Care Cancer. 2014;22(1):163–72. 33. van Ryn M, Phelan S, Arora NK, Haggstrom D, Jackson GL, Zafar Y, Griffin J, Zullig L, Provenzale D, Yeazel M, Jindal R, Clauser S. Patient-reported quality of symptom management among colorectal cancer patients in the VA. J Clin Oncol. 2014;32(8):809–15. 34. Lee JT, Bridges JF, Shockney L. Can pharmacoeconomics and outcomes research contribute to the empowerment of women affected by breast cancer? Expert Rev Pharmacoecon Outcomes Res. 2008;8(1):73–9. 35. Katz SJ, Morrow M. Addressing overtreatment in breast cancer: the doctor’s dilemma. Cancer. 2013;119(20):3584–8. 36. Khoury MJ, Gwinn M, Yoon PW, Dowling N, Moore CA, Bradley L. The continuum of translation research in genome medicine: how can we accelerate the appropriate integration of human genome discoveries into health care and disease prevention? Genet Med. 2007;9:665–74. 37. Birnbaum M. A conversation with Donald Berwick on implementing national health reform. J Health Polit Policy Law. 2012;37(4):709–27. 38. Selby JV, Lipstein SH. PCORI at 3 years—progress, lessons, and plans. N Engl J Med. 2014;370(7):592–5.
Walking in the Shoes of Patients 39. Stange KC, Nutting PA, Miller WL, et al. Defining and measuring the patient-centered medical home. J Gen Intern Med. 2010;25(6):601–12. 40. Bitton A, Martin C, Landon BE. A nationwide survey of patient centered medical home demonstration projects. J Gen Intern Med. 2010;25(6):584–92. 41. Bao Y, Casalino LP, Pincus HA. Behavioral health and health care reform models: patient-centered medical home, health home, and accountable care organization. J Behav Health Serv Res. 2013;40(1):121–32. 42. Larson BK, Van Citters AD, Kreindler SA, et al. Insights from transformations under way at four Brookings-Dartmouth accountable care organization pilot sites. Health Aff (Millwood). 2012;31(11):2395–406. 43. Centers for Medicare and Medicaid Services (CMS), HHS. Medicare program; hospital inpatient prospective payment
systems for acute care hospitals and the long-term care hospital prospective payment system and fiscal year 2014 rates; quality reporting requirements for specific providers; hospital conditions of participation; payment policies related to patient status. Final rules. Fed Regist. 2013;78:50495–1040. 44. Institute of Medicine. Evidence-based medicine and the changing nature of health care: 2007 IOM Annual Meeting Summary. Washington, DC: The National Academies Press; 2008. 45. Stead WW, Lin HS, editors. Computational technology for effective health care: immediate steps and strategic directions. Washington, DC: National Academies Press; 2009. 46. Clauser SB, Wagner EH, Aiello Bowles EJ, Tuzzio L, Greene SM. Improving modern cancer care through information technology. Am J Prev Med. 2011;40(5 Suppl 2):S198–207.
CURRENT OPINION
Walking in the Shoes of Patients, Not Just in Their Genes: A Patient-Centered Approach to Genomic Medicine Neeraj K. Arora • Bradford W. Hesse Steven B. Clauser
•
Ó Springer International Publishing Switzerland (outside the USA) 2014
Abstract Genomic technologies are increasing the precision with which clinicians can assess an individual patient’s risk for developing diseases and identify which patients are likely to benefit from specific treatments. Also advocating for a shift away from a one-size-fits-all approach is the growing emphasis on ‘‘patient-centered’’ care. Using examples from breast cancer, we make a case for why, in order to optimize patient health outcomes, genomic medicine will need to be practiced within a patient-centered framework. We present a six-function conceptual framework for patient-centered care and discuss findings from a national survey evaluating the patientcenteredness of care delivered in the USA.
Key Points for Decision Makers In order to maximize the potential of the genomic revolution in healthcare delivery, genomic medicine needs to be practiced within a patient-centered framework that takes a whole-person approach rather than focusing only on the person’s genes. A six-function conceptual framework for optimizing the patient-centeredness of care has been developed by the National Cancer Institute. National survey data of the American public reveal important deficits in the delivery of patient-centered care on each of the six key functions of patientcenteredness.
1 Introduction
N. K. Arora (&) Division of Cancer Control and Population Sciences, National Cancer Institute, NIH, 9609 Medical Center Drive, 3E514, MSC 9762, Bethesda, MD 20892-9762, USA e-mail: [email protected] B. W. Hesse Division of Cancer Control and Population Sciences, National Cancer Institute, NIH, Bethesda, MD, USA S. B. Clauser Patient-Centered Outcomes Research Institute, Washington, DC, USA
Genomic technologies are increasing the precision with which clinicians can assess patients’ risk for developing diseases and identify which patients are likely to benefit from specific treatments [1]. This new paradigm aims to deliver the right medical interventions to the right patient at the right time [2, 3]. Also advocating for a shift away from a one-size-fits-all approach is the growing emphasis on ‘‘patient-centered’’ care (PCC) [4, 5]. The Institute of Medicine (IOM) defines patient-centeredness as ‘‘providing care that is respectful of and responsive to individual patient preferences, needs, and values, and ensuring that patient values guide all clinical decisions’’ [6, p6]. In order to optimize patient health outcomes, these two paradigms of genomic medicine and PCC will need to be integrated
N. K. Arora et al.
with each other. In this commentary, we present a conceptual framework for facilitating PCC, discuss findings from a recent national survey on the state of patient-centeredness of healthcare in the USA, and, using examples from breast cancer, highlight the salience of facilitating patient-centered aspects of care in a healthcare environment increasingly informed by genomic medicine.
5.
2 Functions of Patient-Centered Care In order to understand the key functions of PCC that will need to be supported by healthcare systems to delivery high-quality care, the National Cancer Institute (NCI) commissioned a thorough review and synthesis of the scientific literature. In their report, authors Epstein and Street [7] outlined a conceptual framework for PCC composed of six critical functions. To stimulate future research, this report also discussed various pathways and mechanisms by which the six PCC functions are likely to impact patient health outcomes [7, 8]. 1.
2.
3.
4.
Fostering healing relationships: In addition to wanting evidence-based medical treatments that are likely to maximize their chances of positive clinical outcomes, patients seek care from clinicians who they can trust and rely on to address their health needs. Clinicians who take the time to know their patient as a person and understand how their illness impacts their daily life are more likely to foster long-term trust. Similarly, healthcare systems that move from a fragmented, ‘‘transaction-focused’’ model of care to a continuous, ‘‘relationship-focused’’ model engender greater patient loyalty while augmenting the value of care provided in service of the ‘‘whole patient’’ [9, 10]. Exchanging information: Patients need support from clinicians to make sense of complex medical information that they may obtain from multiple sources. Healthcare systems need to provide medical information in a manner that is easily understood and retained by patients. They also need to inculcate active listening skills to help patients feel comfortable in disclosing personal information that may be important for decision making. Facilitating decision making: While a trusting relationship and information exchange are important for decision making, to facilitate informed decision making, clinicians also need to support patients in their own decisional deliberations by helping them think through their values and preferences as they jointly evaluate various medical options. Responding to emotions: Being at a high risk for, or living with, a potentially life-threatening and/or long-
6.
term chronic illness can result in significant patient distress. To enhance patients’ emotional well-being, clinicians need to reliably assess patients’ distress, legitimize their feelings, show empathy, and where possible provide patients with tangible help to address their negative emotions. Enabling self-management: Given that a large majority of patient care takes place outside the healthcare setting, patients need support from the healthcare system in preparing them for taking care of their health in between visits. This includes support for care coordination, managing symptoms and side effects, engaging in healthy lifestyles, and ensuring adherence to treatments. Managing uncertainty: Patients experience a range of illness-related uncertainties that are scientific, personal, or practical in nature and can significantly impact their well-being [11]. Clinicians need to be aware of patients’ feelings of uncertainty and manage them by facilitating the other five functions of PCC.
3 Walking in the Shoes of Patients To evaluate the state of ‘‘patient-centeredness’’ from the perspective of patients in the general US population, we developed, tested, and included six questions addressing the six PCC functions for administration in the NCI’s Health Information National Trends Survey (HINTS 4, cycle 1). The HINTS program was launched by the NCI in 2001 as a means for assessing the diffusion of health communication messages and strategies at a time of extraordinary change in the overall health information environment [12]. The original program was designed to administer computer-assisted telephone interviews biennially through a list-assisted, random-digit-dial survey of non-institutionalized adults in the USA over 18 years of age. Because of falling response rates among telephone surveys and the increased pace of change in communication technology, the NCI reengineered the survey to be administered by paper and pencil using a randomly drawn sample of addresses from a list of US postal addresses and to be administered over a series of four cycles over a 3-year period [13, 14]. The first cycle of the newly reengineered survey was in the field from October 25, 2011 to February 7, 2012; data from this survey are discussed below. A series of 50 replicate weights were generated to account for the complex survey design and to adjust prevalence estimates based on post-stratification adjustments from census data. The PCC questions asked respondents to report their experiences of how often in the past 12 months their providers addressed each of the six PCC functions
Walking in the Shoes of Patients
(N = 3,322; see Fig. 1 for exact item wording). As shown in Fig. 1, a large proportion of the American population reported that they ‘‘always’’ received PCC (45–61 % across the six functions). However, several deficiencies were reported. Our data show that one out of every four Americans (23 %) who received healthcare in the USA reported that their healthcare providers rarely (never or sometimes) paid attention to their emotions, almost one in five (18 %) were rarely involved in decision making as much as they wanted, and one in four rarely received help in dealing with feelings of uncertainty about their health or healthcare. Our data also suggest that at least one in ten Americans are unable to ask all of their health-related questions during medical visits, they rarely understand the things they need to do to take care of their health once they leave the doctor’s office, and they feel they cannot rely on the healthcare system to take care of their healthcare needs. We contend that in a highquality healthcare delivery system, we should be 95 % confident that patients will receive PCC most of the time, if not all the time (usually or always). Thus, the error rate in delivering sub-optimal PCC should be no more than 5 % compared with the current levels of 11–26 % (i.e., those who had a response of never or sometimes across the six patient-centered functions in our survey). Similar findings highlighting room for improvement in delivering PCC have been reported recently by the IOM [15].
4 Patients’ Care Experiences and Genomic Medicine While our national data suggest the need to optimize the six PCC functions in general, the impetus for doing so is especially high when we consider applications of genomics in clinical practice. To illustrate how the six-function framework may serve to support patient-centeredness in an environment enabled by genomic medicine, we consider two common applications of genomics related to germline genomic testing for breast cancer disease risk prediction and somatic genomic testing for predicting risk of breast cancer recurrence and individualizing chemotherapy treatment decisions [16]. 4.1 Disease Risk Prediction Approximately 5–10 % of all breast cancers have a genetic component associated with them [17]. The most common cause of hereditary breast cancer is a mutation in either the BRCA1 or BRCA2 gene. A BRCA1 or BRCA2 mutation results in a substantial increase in lifetime risk of breast cancer from 12 % for the average woman to 50–60 % for those with a mutation [18]. Interest in BRCA testing has soared significantly since 2013, after actress and director Angelina Jolie reported in the New York Times that she had the BRCA1 mutation and underwent preventive double mastectomy to reduce her risk of dying from breast cancer [19, 20]. Primary care providers and genetics specialists reported what has been termed ‘‘the Angelina Jolie effect,’’
70 61
60
Weighted Percentage
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54
52
50
45 41
40 32
30 20
26
33
33 30
29 26
23 18
14
13
11
10 0
Informaon
Emoons
Decisions
Self Mgt
Uncertainty Relaonships
Funcons of Paent-Centered Care (PCC)* Never/Somemes
Fig. 1 Weighted percentage of US adults’ reports on the patientcenteredness of healthcare delivery in the U.S. *Data were collected as part of the National Cancer Institute’s 2012 Health Information National Trends Survey (HINTS4, cycle 1). Responders who saw a healthcare provider in the past 12 months (N = 3,322) were asked to report on their PCC experiences in the past 12 months on a never, sometimes, usually, always scale. The following six PCC questions were asked: 1. Fostering healing relationships: How often did you feel you could rely on your healthcare providers to take care of your healthcare needs? 2. Exchanging information: How often did your
Usually
Always
providers give you the chance to ask all the health-related questions you had? 3. Facilitating decision making: How often did your providers involve you in decisions about your health care as much as you wanted? 4. Responding to emotions: How often did your providers give the attention you needed to your feelings and emotions? 5. Enabling self-management: How often did your providers make sure you understood the things you needed to do to take care of your health? 6. Managing uncertainty: How often did your providers help you deal with feelings of uncertainty about your health or health care?
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a surge in queries from women across the country on whether they should receive BRCA testing and/or undergo bilateral mastectomy [18, 21]. The typical process related to testing for BRCA mutations in many comprehensive cancer centers that have dedicated clinical genetics clinics may involve two face-toface meetings with the patient, first to assess the appropriateness of BRCA testing by conducting a comprehensive assessment of family cancer history followed by a consultation with a trained genetic counselor for those women for whom BRCA testing may be appropriate [22]. To derive maximum benefit from BRCA testing on short- and longterm patient outcomes, clinical teams interacting with patients and family members will have to provide them with ongoing support addressing several needs related to PCC during these initial visits and beyond. For example, women without a personal history of breast cancer who test positive for BRCA1 or BRCA2 mutation face several complex choices for early detection and/or risk reduction. These include yearly screening with mammography and breast magnetic resonance imaging (MRI), chemoprevention with tamoxifen, and surgical options, including prophylactic mastectomy [18, 22–24]. Each of these approaches has its own downsides. Annual cancer screening can result in significant psychological distress, especially given false positive results that may be encountered in breast MRI screening. Side effects of surgical and pharmacological interventions include implications for body image, early menopause, fertility and sexual functioning problems, weight gain, and increased risk of cardiovascular disease [18, 22–24]. Unlike the case of women diagnosed with invasive breast cancer, women who test positive for BRCA mutations should not, in most cases, feel a time pressure to make a treatment or surveillance decision within the context of one or two initial medical visits. These women and their family members need coordinated, ongoing support from the multiple providers they are likely to see during this time, including genetic counselors, primary care physicians, and oncology specialists, in weighing the risks and benefits of different approaches and incorporating their values and preferences in decisions that are likely to have significant long-term implications for their life [24]. Moreover, given the several side effects associated with various options, clinical teams will have to recognize and address those physical, emotional, and social functioning problems over time in a way that minimizes decision regret among patients. Women found to carry a BRCA mutation will also need additional counseling and support from their clinical teams to facilitate communication with their family members about the implication of the test results on their family [18]. Population level studies are needed to assess the extent to which women receive ongoing support,
beyond initial genetic counseling consultations, from a coordinated, healthcare system to meet their various medical and psychosocial needs. 4.2 Individualizing Chemotherapy Treatment Nearly 50 % of breast cancers diagnosed in the USA are early-stage, estrogen receptor-positive, lymph node-negative cancers. Many patients with such a diagnosis receive adjuvant chemotherapy and experience debilitating side effects despite limited survival benefits [25]. To improve individualizing of adjuvant treatments, gene expression profiling (GEP) of breast tumors using tests such as the Oncotype DxTM, a 21-gene assay, is being used to identify women who are more likely to benefit from chemotherapy on the basis of their recurrence risk scores (RSs) [26, 27]. A systematic review and meta-analysis of 23 studies on the impact of Oncotype DxTM on clinical practice shows that a little less than half of all patients who take the test receive a low RS, 39 % receive an intermediate RS, and 12 % receive a high RS [25]. In at least one in three cases, the Oncotype DxTM results have been shown to change the clinician’s prior recommendations related to adjuvant chemotherapy. While GEP tests like the Oncotype DxTM hold significant promise to individualize chemotherapy decisions, similar to our observations for germline genomic testing using the example of BRCA mutations, several patient needs related to the six patient-centered functions will have to be systematically addressed to maximize benefit from these tests. A limited number of studies have examined patient experiences with GEP and its impact on their treatment decision making. Bombard et al. [28] reported from their qualitative findings that many women misunderstood the purpose of the test, some reported information overload while receiving the test results, and many considered the GEP test to provide them with the most definitive information to facilitate their chemotherapy decision. Similarly, Tzeng et al. [26] reported a third of their sample lacked a complete understanding of the discussions they had related to GEP and one in four experienced distress related to the test results. The authors suggest there is a great need to aid and improve risk communication and decision making within the context of using GEP for adjuvant chemotherapy decisions. Depending upon the recurrence RS, specific patientcentered issues will need to be addressed. For example, women with high RSs are likely to choose chemotherapy. In addition to knowing their RS, they will need adequate information about expected short- and long-term side effects in a way they can easily understand. Knowledge of a higher probability of recurrence and anticipation of chemotherapy-related side effects can result in significant distress that will need to be addressed by clinical teams. While undergoing chemotherapy, patients will need self-
Walking in the Shoes of Patients
management support to manage their symptoms and side effects at home. While several national efforts have been made to integrate palliative care for patients from the time of diagnosis and there exists a large evidence base for many interventions that clinical teams can use to evaluate and manage a variety of patient symptoms [29, 30], several studies continue to report significant short- and long-term unmet symptom needs experienced by cancer patients and survivors [31–33]. The benefit of chemotherapy for the many patients who receive an intermediate RS is not clear. The clinical uncertainty of the test result needs to be communicated to these women in a manner that minimizes distress. Clinicians will need to support them in thinking through their values and preferences while making the decision about chemotherapy in the face of uncertainty. Interventions grounded in decision analysis that facilitate elicitation and clarification of patient preferences can help optimize patient–clinician communication and enhance patient engagement [28, 34, 35]. For patients who decide against chemotherapy, long-term distress related to fear of recurrence needs to be recognized and addressed. Women with low RSs are unlikely to choose chemotherapy and many consider the GEP test to be their savior rescuing them from experiencing unnecessary side effects [28]. However, these women still need ongoing surveillance to monitor for late effects of other treatments and for secondary malignancies. Clinicians will need to engage them in developing and implementing a survivorship care plan to facilitate such surveillance and promote a healthy lifestyle. Khoury et al. [36] describe four phases of translational genomics that move from basic genomic discoveries to candidate health applications (T1), to assessing the value of the genomic applications for clinical practice leading to development of evidence-based guidelines (T2), to implementing the guidelines in clinical practice (T3), to evaluating the impact of genomic applications on individual and population health outcomes (T4). Bombard et al. [16] note that significant gaps currently exist in the evidence base for genomics applications to successfully move from T1 to T4 and call for more focused research in several areas, including outcomes and health services research. As we have illustrated in the examples above, in order to maximize the impact of genomic applications on patient health outcomes, explicit efforts will need to be made to incorporate the patient’s perspective in genomics translational research as well as in clinical practice. 5 Conclusion As efforts towards implementing the Patient Protection and Affordable Care Act unfold [37], an emphasis on
patient-centeredness is likely to increase in research and practice, as evidenced by the establishment of the PatientCentered Outcomes Research Institute (PCORI) [38] and implementation of innovative models of care such as the patient-centered medical home [39, 40] and accountable care organizations [41, 42]. Even at the policy level, a focus on delivering PCC is being incorporated in payment models. For example, the Centers for Medicare & Medicaid Services’ implementation of a value-based purchasing program proposes to reimburse hospitals in part on their performance on patient-reported, patient-centered measures [43]. At the same time, genomically informed medicine is creating an environment that is awash in a deluge of data. In a report on evidence-based medicine by the IOM, authors recounted the observation that in 1990 a typical clinician or patient would have to bear roughly five to seven individual facts in mind in order to give due diligence to a treatment decision. By 2020, with the burgeoning availability of structural data on haplotypes and single nucleotide polymorphisms, the documentation of gene expression profiles, and a more thorough assessment of proteomic and effector molecules, the number of individual facts to consider for a precision-based treatment decision will likely exceed 1,000 [44]. Clearly, innovation will be needed to package this information and to reengineer clinical care processes so as to not outstrip the capacities of physicians, care teams, genetic counselors, patients, and caregivers [45, 46]. The goal in this new world is to engineer a system that follows the functional requirements of the PCC framework as articulated earlier; that is, to create a system with 95 % effectiveness in meeting patients’ expectations for a healing relationship in which they exchange information effectively, cope with uncertainty, clarify their emotions, make value-congruent decisions, and are effective in self-management. In an era of healthcare reform and genomic medicine, patient health outcomes are likely to be optimized when we take a comprehensive approach from the patient’s genes to the whole patient. In this new paradigm, healthcare systems will need to support clinical teams in their efforts to facilitate the patient-centered aspects of care, for we must not forget the patient in the pursuit of his or her genes. Acknowledgments This article reflects the personal opinions of the authors and does not necessarily represent any official position of the National Cancer Institute, National Institutes of Health, or the PatientCentered Outcomes Research Institute. The authors wish to thank Muin Khoury, MD, PhD for his helpful feedback on an initial draft of the manuscript. Conflict of Interest interest.
None of the authors have any conflict of
N. K. Arora et al. Authors contribution All authors contributed to the conceptualization, writing, and final approval of the manuscript.
References 1. Institute of Medicine. The value of genetic and genomic technologies: workshop summary. Washington, DC: The National Academies Press; 2010. 2. Collins FS, Guttmacher AE. Genetics moves into the medical mainstream. JAMA. 2001;286(18):2322–4. 3. Issa AM. Personalized medicine and the practice of medicine in the 21st century. Mcgill J Med. 2007;10(1):53–7. 4. Epstein RM, Fiscella K, Lesser CS, Stange KC. Why the nation needs a policy push on patient-centered health care. Heath Aff (Millwood). 2010;29:1489–95. 5. Davis K, Schoenbaum SC, Audet AM. A 2020 vision of patientcentered primary care. J Gen Intern Med. 2005;20(10):953–7. 6. Institute of Medicine. Crossing the quality chasm: a new health system for the 21st century. Washington, DC: National Academies Press; 2001. 7. Epstein RM, Street RL, Jr. Patient-centered communication in cancer care: promoting healing and reducing suffering. Bethesda: National Cancer Institute, NIH publication no. 07-6225; 2007. 8. Street RL Jr, Makoul G, Arora NK, Epstein RD. How does communication heal? Pathways linking clinician-patient communication to health outcomes. Patient Edu Couns. 2009;74:295–301. 9. Zuboff S, Maxmin J. The support economy: why corporations are failing individuals and the next episode of capitalism. New York: Viking; 2002. p. 2002. 10. Institute of Medicine. Cancer care for the whole patient: meeting psychosocial health needs. Washington, DC: The National Academies Press; 2008. 11. Han PKJ, Klein WMP, Arora NK. Varieties of uncertainty in healthcare: a conceptual taxonomy. Med Decis Making. 2011;31:828–38. 12. Nelson DE, Rimer BK, Kreps GL, Hesse BW, Viswanath KV, Croyle RT, Willis G, Arora NK, Weinstein N, Alden S. The Health Information National Trends Survey (HINTS): development, design, and dissemination. J Health Commun. 2004;9:1–18. 13. Finney Rutten LJ, Davis T, Beckjord EB, Blake K, Moser RP, Hesse BW. Picking up the pace: changes in method and frame for the Health Information National Trends Survey (2011–2014). J Health Commun. 2012;17:979–89. 14. Rutten LJF, Hesse BW, Moser RP, Kreps GL, editors. Building the Evidence Base in Cancer Communication. Cresskill: Hampton Press; 2011. 15. Novelli WD, Halvorson GC, Santa J. Recognizing an opinion: findings from the IOM evidence communication innovation collaborative. JAMA. 2013;308:1531–2. 16. Bombard Y, Bach PB, Offit K. Translating genomics in cancer care. J Natl Compr Cancer Netw. 2013;11(11):1343–53. 17. Nelson HD, Huffman LH, Fu R, Harris EL. U.S. Preventive Services Task Force. Genetic risk assessment and BRCA mutation testing for breast and ovarian cancer susceptibility: systematic evidence review for the U.S. Preventive Services Task Force. Ann Intern Med. 2005;143(5):362–79. 18. McCarthy AM, Armstrong K. The role of testing for BRCA1 and BRCA2 mutations in cancer prevention. JAMA Intern Med. 2014;174(7):1023–4. 19. Jolie A. My medical choice. The New York Times. http://www. nytimes.com/2013/05/14/opinion/my-medical-choice.html. 14 May 2013.
20. Neporent L. Angelina Jolie’s double mastectomy fueling national debate. http://abcnews.go.com/Health/angelina-jolies-doublemastectomy-fueling-national-debate/story?id=19315336. 4 June 2013. 21. Matloff ET. The Angelina effect: rising interest in genetic testing creates opportunities for patients—and profit. Am J Manag Care. 2014;20(special issue 3):SP67. 22. Connors LM, Voian N, Shi Y, Lally RM, Edge S. Decision making after BRCA genetic testing: down the road of transition. Clin J Oncol Nurs. 2014;18(3):E58–63. 23. Hesse-Biber S. The genetic testing experience of BRCA-positive women: deciding between surveillance and surgery. Qual Health Res. 2014;24(6):773–89. 24. Stan DL, Shuster LT, Wick MJ, Swanson CL, Pruthi S, BakkumGamez JN. Challenging and complex decisions in the management of the BRCA mutation carrier. J Womens Health. 2013;22(10):825–34. 25. Carlson JJ, Roth JA. The impact of the Oncotype Dx breast cancer assay in clinical practice: a systematic review and metaanalysis. Breast Cancer Res Treat. 2013;141(1):13–22. 26. Tzeng JP, Mayer D, Richman AR, et al. Women’s experiences with genomic testing for breast cancer recurrence risk. Cancer. 2010;116:1992–2000. 27. Lo SS, Mumby PB, Norton J, et al. Prospective multicenter study of the impact of the 21-gene recurrence score assay on medical oncologist and patient adjuvant breast cancer treatment selection. J Clin Oncol. 2010;28(10):1671–6. 28. Bombard Y, Rozmovits L, Trudeau ME, Leighl NB, Deal K, Marshall DA. Patients’ perceptions of gene expression profiling in breast cancer treatment decisions. Curr Oncol. 2014;21(2):e203–11. 29. Institute of Medicine. Improving Palliative Care for Cancer: Summary and Recommendations. Washington, DC: The National Academies Press; 2001. 30. Loprinzi CL, Wolf SL, Barton DL, Laack NN. Symptom management in premenopausal patients with breast cancer. Lancet Oncol. 2008;9(10):993–1001. 31. Yoon J, Malin JL, Tisnado DM, Tao ML, Adams JL, Timmer MJ, Ganz PA, Kahn KL. Symptom management after breast cancer treatment: is it influenced by patient characteristics? Breast Cancer Res Treat. 2008;108(1):69–77. 32. Kent EE, Mitchell SA, Oakley-Girvan I, Arora NK. The importance of symptom surveillance during follow-up care of leukemia, bladder, and colorectal cancer survivors. Support Care Cancer. 2014;22(1):163–72. 33. van Ryn M, Phelan S, Arora NK, Haggstrom D, Jackson GL, Zafar Y, Griffin J, Zullig L, Provenzale D, Yeazel M, Jindal R, Clauser S. Patient-reported quality of symptom management among colorectal cancer patients in the VA. J Clin Oncol. 2014;32(8):809–15. 34. Lee JT, Bridges JF, Shockney L. Can pharmacoeconomics and outcomes research contribute to the empowerment of women affected by breast cancer? Expert Rev Pharmacoecon Outcomes Res. 2008;8(1):73–9. 35. Katz SJ, Morrow M. Addressing overtreatment in breast cancer: the doctor’s dilemma. Cancer. 2013;119(20):3584–8. 36. Khoury MJ, Gwinn M, Yoon PW, Dowling N, Moore CA, Bradley L. The continuum of translation research in genome medicine: how can we accelerate the appropriate integration of human genome discoveries into health care and disease prevention? Genet Med. 2007;9:665–74. 37. Birnbaum M. A conversation with Donald Berwick on implementing national health reform. J Health Polit Policy Law. 2012;37(4):709–27. 38. Selby JV, Lipstein SH. PCORI at 3 years—progress, lessons, and plans. N Engl J Med. 2014;370(7):592–5.
Walking in the Shoes of Patients 39. Stange KC, Nutting PA, Miller WL, et al. Defining and measuring the patient-centered medical home. J Gen Intern Med. 2010;25(6):601–12. 40. Bitton A, Martin C, Landon BE. A nationwide survey of patient centered medical home demonstration projects. J Gen Intern Med. 2010;25(6):584–92. 41. Bao Y, Casalino LP, Pincus HA. Behavioral health and health care reform models: patient-centered medical home, health home, and accountable care organization. J Behav Health Serv Res. 2013;40(1):121–32. 42. Larson BK, Van Citters AD, Kreindler SA, et al. Insights from transformations under way at four Brookings-Dartmouth accountable care organization pilot sites. Health Aff (Millwood). 2012;31(11):2395–406. 43. Centers for Medicare and Medicaid Services (CMS), HHS. Medicare program; hospital inpatient prospective payment
systems for acute care hospitals and the long-term care hospital prospective payment system and fiscal year 2014 rates; quality reporting requirements for specific providers; hospital conditions of participation; payment policies related to patient status. Final rules. Fed Regist. 2013;78:50495–1040. 44. Institute of Medicine. Evidence-based medicine and the changing nature of health care: 2007 IOM Annual Meeting Summary. Washington, DC: The National Academies Press; 2008. 45. Stead WW, Lin HS, editors. Computational technology for effective health care: immediate steps and strategic directions. Washington, DC: National Academies Press; 2009. 46. Clauser SB, Wagner EH, Aiello Bowles EJ, Tuzzio L, Greene SM. Improving modern cancer care through information technology. Am J Prev Med. 2011;40(5 Suppl 2):S198–207.
