ORIGINAL ARTICLE
Focusing on the “Person” in Personalized
Medicine: The Future of Patient-Centered
Care in Radiation Oncology
Abigail T. Berman, MD, MSCE a , Seth A. Rosenthal, MD b, Drew Moghanaki, MD, MPH c,
Kristina D. Woodhouse, MD a, Benjamin Movsas, MD d, Neha Vapiwala, MD a
Abstract
Numerous efforts in radiation oncology aim to improve the value of clinical care. To evaluate the success of these efforts, outcome
measures must be well defined and incorporate the beliefs of the patients they affect. These outcomes have historically centered on rates
of tumor control, overall survival, and adverse events as perceived and reported by providers. However, the future of patient-centered
care in radiation oncology is increasingly focusing on the “person” in the population and the individual in the studies to more closely
reflect the ideals of personalized medicine. Formally known as patient-centered outcomes, this metric encompasses parameters of patient
satisfaction, engagement, and treatment compliance. Evaluations that investigate the safety and efficacy of treatments are increasingly
soliciting participation from patients within a model of shared decision making that improves patients’ knowledge, satisfaction, physical
and emotional well-being, and trust in providers. Modern clinical trials that embrace this approach may even focus on patient-reported
outcomes as the primary end point, as opposed to time-honored physician-reported events. The authors explore the growing role of
patient-centered care, the incorporation of shared decision making, and the relevant body of existing and developing literature on this
topic in radiation oncology. The authors report recent discoveries from this area of study and describe how they can not only support
high-quality, high-value patient care but also enhance recruitment to clinical oncology trials, both of which are challenging to achieve in
today’s relatively resource-strapped environment.
Key Words: Radiation oncology, shared decision making, personalized care, decision aid, quality of life, patient-reported outcomes
J Am Coll Radiol 2016;13:1571-1578. Copyright 2016 American College of Radiology
INTRODUCTION
What is personalized care in radiation oncology?
Although molecular genomics have revolutionized
medical oncologists’ ability to distinguish which
chemotherapy or targeted agent best suits any individual
patient, defining the “personal” patient characteristics
that drive decisions to use radiation, and, if so, what
type and how much, remain ill defined at present.
a
Department of Radiation Oncology, University of Pennsylvania, Philadelphia, Pennsylvania.
b
Sutter Medical Group and Sutter Cancer Center, Sacramento, California.
c
Virginia Commonwealth University, Richmond, Virginia.
d
Henry Ford Hospital, Detroit, Michigan.
Corresponding author and reprints: Abigail T. Berman, MD, MSCE,
Department of Radiation Oncology, Hospital of the University of Pennsylvania, 3400 Civic Center Boulevard, Philadelphia, PA 19104; e-mail:
[email protected].
The authors have no conflicts of interest related to the material discussed in
this article.
ª 2016 American College of Radiology
1546-1440/16/$36.00 n http://dx.doi.org/10.1016/j.jacr.2016.09.012
Radiation oncology historically has been a field rooted in
patient-centered care, with an engrained drive to achieve
optimal efficacy against the target, whether for cure or
palliation, with minimal morbidity to patients.
Although ostensibly this dual-sided but complementary
drive has focused on technological innovation, the
nontechnical advancements are equally if not perhaps
more important to patient satisfaction, engagement,
compliance, and ultimately outcomes. Shared decision
making (SDM), with or without the use of clinical decision aids (DAs), holds the promise of providing the
degree of personalization and patient-centered care for
patients in their journey toward discovering the most
appropriate radiation treatment plan, including whether
radiation is at all appropriate or the modality used. In
addition, outcomes research in radiation oncology is
increasingly moving to a patient-centered era, with the
incorporation of patient-reported adverse events as preeminent end points.
1571
SDM IN ONCOLOGY PERMITS
PATIENT-CENTERED CARE
SDM, or the active involvement of patients in considering and ultimately deciding upon their treatment plans
jointly with their health care providers, is not a new
concept but rather was defined in the late 1990s by
Charles et al [1]. Their revised framework, published in
1999, espoused the key hallmarks of SDM as a process
that
(1) explicitly identifies different analytic steps in the
treatment decision-making process; (2) provides a
dynamic view of treatment decision-making by
recognizing that the approach adopted at the outset
of a medical encounter may change as the interaction evolves; (3) identifies decision-making approaches which lie between the three predominant
models (paternalistic, shared and informed); and
(4) has practical applications for clinical practice,
research and medical education.
Most importantly, the model identifies that patient
preferences are taken into account, which previously was
not formally recognized in the literature. The concept of
SDM has been supported by many national organizations, including NRG Oncology, the American Society of
Clinical Oncology, and the Patient-Centered Outcomes
Research Institute, which have funded more than 71
comparative clinical effectiveness research studies focused
on SDM [2].
Despite this formal definition, there is significant
variability in the definition of SDM. The Informed
Medical Decisions Foundation defines six steps of SDM,
but the steps are broadly defined: invite the patient to
participate, present options, provide information on
benefits and risks, assist patients in evaluating options on
the basis of their goals and concerns, facilitate deliberation and decision making, and implement SDM [3,4].
One group developed an oncology-specific SDM coding
system, the Decision Analysis System for Oncology, in
early-stage breast cancer, a topic for which there are
ample data that patients wish to be actively involved in
surgical choice yet are inadequately involved [5]. The
investigators found it to be reliable and valid compared
with other recognized SDM coding systems such as the
OPTION and the Decision Support Analysis Tool [6].
Generally, SDM has been touted for its potential to
create more informed patients and family members and
to increase trust in the physician-patient relationship.
Nonetheless, there have been barriers to physicians using
SDM. A German group investigated these challenges
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using quantitative analysis and found that time and
structural constraints and a lack of (multidisciplinary)
communication were the most negative aspects of
SDM [7].
For the past two decades, groups have investigated the
use of SDM to improve patient-centered care [7].
However, few studies have examined SDM in radiation
oncology specifically. Shabason et al [8] explored the
association between SDM and patient satisfaction
during radiotherapy. Interestingly, they found that only
about one-third of patients experienced SDM or
perceived control in treatment decisions and that these
metrics correlated with patient satisfaction. In addition,
anxiety, depression, and fatigue were greater in patients
who desired but did not perceive control over their
treatments.
PATIENT-CENTERED SDM MODELS IN
RADIATION ONCOLOGY
SDM models have been conceptually developed, as outlined previously, yet the exact mechanism and features
that distinguish them from typical office visits are still
being defined. A detailed discussion about the risks and
benefits of one treatment over another can constitute
SDM, but the most formalized approach is the use of a
DA, which can be presented as a printed handbook, a
video, or an interactive electronic guide. Clear hallmarks
of a DA include a detailed, personalized discussion of
treatment options within the context of a patient’s specific demographics, disease-related features, and personal
beliefs to help prioritize the patient’s values and goals.
The International Patient Decision Aids Standards
collaboration has helped define the required elements of a
DA. Even in groups of physicians who believe they are
using SDM, a minority are using DAs [9]. Like SDM as
an overall concept, DAs in oncology also have been
proved to promote higher quality decisions [10], patient
knowledge, patient-provider communication, patient
participation, and decisional satisfaction [11,12]. The
largest barrier to routine DA implementation is the
system-level support, staffing, and time needed to make
DAs part of routine clinical care [11,13]. Embedding
DAs into the electronic health record (EHR) has a
multitude of potential benefits: (1) it reliably extracts all
pertinent clinical information, (2) it prompts providers
to offer the use of DAs, (3) it allows sharing of the DA
results with the patient through a secure patient portal,
and (4) it enables real-time clinical decision support for
patients and providers on the basis of the DA results [4].
Despite these benefits, few EHRs are currently able to
Journal of the American College of Radiology
Volume 13 n Number 12PB n December 2016
accommodate because of the need to merge multiple IT
platforms and variable standardization of data elements.
As the informatics infrastructure accommodates the use
of DAs, it will be critical to embed their use into
clinical pathways. Centers that have successfully
integrated DAs into the electronic medical record
requires desire and interest by key members of any
multidisciplinary group, dissemination to all members,
and feedback and accountability on system use and
performance, based on either “peer pressure” or
financial-based incentives [14].
MEASURING THE SUCCESS OF SDM IN
RADIATION ONCOLOGY
The appropriate end point of trials investigating SDM is
controversial; what is the best surrogate end point or
metric for patient-centered care? Brundage et al [15]
outlined short- versus long-term outcomes, including
shorter term provider and patient outcomes (satisfaction
with decision-making process and patient-provider partnership, confidence in decision, patient trust in provider,
self-efficacy, mental health, physical and emotional wellbeing) and longer term patient outcomes (treatment
adherence, quality of life (QOL), and remission). Internationally, Germany adopted SDM as part of new melanoma guidelines and used a longitudinal questionnaire
to determine the value, finding that more than 80% of
patients, according to the Control Preference Scale,
wanted to play an active role and found a preference shift
in 43% of patients toward active involvement [16].
Perhaps the strongest end point of the use of SDM has
been shown in palliative care, in which SDM decreased
the odds of receiving chemotherapy in the last 14 days
of life and of dying in an acute care setting, two wellvalidated markers of higher quality palliative care [12].
In radiation oncology, it is unclear what the best metric
of success using SDM will be. Patient satisfaction, trust
in providers, and physical emotional well-being are
consistently useful metrics; it is not yet established the
best way to integrate these metrics into alternative payment models, but there are a variety of pilot programs
using these tools as part of reimbursement strategies [17].
CURRENT RADIATION ONCOLOGY TRIALS IN
SDM AND DAs
In the contemporary radiation oncology environment,
any additional steps to routine clinical care must be
clearly justified by validated research. Research programs
evaluating SDM and the value of DAs have been
Journal of the American College of Radiology
Berman et al n Personalized Medicine
increasing steadily, with four recently completed or
currently open trials (as of July 5, 2016) evaluating the
utility of DAs as their primary method (Table 1). The
primary end points of these studies include decisional
conflict scale scores, self-efficacy, uncertainty, and
knowledge and preference scores.
QOL AND PATIENT-REPORTED OUTCOMES IN
RADIATION ONCOLOGY CLINICAL TRIALS
A focus on QOL has been a central premise of radiation
oncology practice for many years and represents a way in
which patient-centered care has been integral to radiation
oncology practice. RTOG and its successor organization, NRG Oncology, have been frontrunners in this
regard. For example, prior RTOG studies have demonstrated that QOL significantly predicts outcomes,
including local control and survival [18-20]. QOL has
also helped better define the potential role and benefit
of more sophisticated technologies in radiation
oncology, such as intensity-modulated radiation therapy
(RT) [21]. Furthermore, the importance of considering
family support networks to cancer survival was
demonstrated by Konski et al [22], who noted that
men without partners had inferior survival on
multivariate analysis compared with married men or
other men with partners. Metrics and methods
developed by RTOG have helped establish the
centrality of patient- and family-centered care in the
practice of radiation oncology.
Increased recognition of the importance of patientreported outcomes (PROs) is another way that patientcentered care has been translated into radiation
oncology. PROs have been recognized for more than a
decade, but unlike more traditional oncologic end points,
widespread adoption of PROs has been hampered by
inconsistency in terminology and use. Patient toxicity has
typically been reported by the provider-generated National Cancer Institute (NCI) Common Toxicity Common Terminology Criteria for Adverse Events (CTCAE).
However, multiple studies have shown the discordance
between provider and patient toxicity reporting [23,24],
and therefore there has been a priority to make PROs a
critical end point in many studies, particularly
comparative effectiveness research. More recently, this
important metric has begun to take a preeminent
position as a validated end point in many trials [25].
There are multiple validated PRO instruments,
including the European Organization for Research and
Treatment of Cancer Quality of Life Questionnaire
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Table 1. Current radiation oncology trials using shared decision making and decision aids
Study Name
Malignancy
A Breast Cancer Treatment
Early-stage breast
Decision Aid for Women Aged
cancer
70 and Older
Testing Decision Aids About
Early Stage Prostate Cancer
Early-stage prostate
cancer
Impact of Radiation Therapy on DCIS
Breast Conservation in DCIS
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Volume 13 n Number 12PB n December 2016
Use of a Video Decision Tool to Hospitalized patients
eligible for palliative
Improve Informed DecisionRT
Making in Hospitalized
Patients Considering Palliative
Radiation Therapy
Early-stage operable
Improving Shared Decisionor borderline lung
Making in Cancer Care: A
cancer
Personalized, Electronic
Decision Aid for Patients with
Early Stage Lung Cancer
Recruitment
Goal
312
564
35,000
43
150
Treatment
Primary End Point
Decision
Decisional Conflict Mastectomy vs
Scale
BCS, RT after
BCS, and
hormonal
therapies
Video DA in
Self-efficacy for
addition to
discussing
written materials
preferences
regarding active
surveillance,
surgery,
radiation
Long-term breast
Patients with DCIS
conservation
who undergo
BCS not
followed by RT
Choice of palliative
Uncertainty,
RT
knowledge and
preference
scores
Decisional conflict
SBRT vs surgery
Open Date
June 2016
December 2015
Primary
Institution
Status
Dana Farber Cancer Open, not recruiting
Institute
University of
Michigan
September 2012
Completed
Hold
August 2012
Dana Farber Cancer Completed
Institute
March 2016
University of
Pennsylvania
Note: BCS ¼ breast-conserving surgery; DA ¼ decision aid; DCIS ¼ ductal carcinoma in situ; RT ¼ radiation therapy; SBRT ¼ stereotactic body radiation therapy.
Open
Core QLQ-C30, the Functional Assessment of Cancer
Therapy, the MD Anderson Symptom Inventory, the
Patient-Reported Outcomes Measurement Information
System, and, most recently, PRO-CTCAE [23]. PROCTCAE was developed starting in 2008 to decrease
heterogeneity in patient-centered data after careful analysis by the NCI, with the purpose of complementing
existing safety and tolerability assessments across cancer
clinical trials [26,27]. This measurement has been
analyzed as a valid, reliable, and responsive instrument,
and results are favorable in a diverse population and in
comparison with other QOL scale changes [28,29].
Limitations of the PRO-CTCAE include lack of validation in surgical and non-English-speaking patients.
Ultimately, a key goal is for PROs to be a primary end
point in appropriate clinical trials to define the next
standard of care based directly on patients’ perspective.
For example, in treatment comparisons that are hypothesized to have no significant difference in traditional
objective clinical outcomes, such as progression-free survival, PROs can be a useful primary end point in trials if
it is hypothesized that the two treatments have different
adverse events or other clinically relevant outcomes, such
as fewer missed work days or preservation of ability to
work. Indeed, in radiation oncology, more studies are
being designed precisely this way [24]. RTOG has
ongoing trials in which PRO end points are not only
integral elements of the studies but are in fact the
primary objectives. For example, RTOG 0938 (A
Randomized Phase II Trial of Hypofractionated
Radiotherapy for Favorable Risk Prostate Cancer) is a
randomized
phase
2
trial
comparing
two
hypofractionated radiation regimens. The bladder and
bowel domains of the Expanded Prostate Cancer Index
Composite instrument are being used to measure
health-related QOL as the primary end point of that
study. The trial has been completed, design of the successor trial is under way, and QOL outcomes will be an
important part of the new trial [30]. The Prostate
Advanced Radiation Technologies Investigating Quality
of Life trial is an exciting example of a randomized
study to incorporate a sole PRO (Expanded Prostate
Cancer Index Composite bowel score) as the primary
end point [31]. In addition, QOL holds the promise of
enhancing clinical care as a method of communication
from patients to providers to communicate symptoms
that need to be addressed in real time [32]. More and
more, efforts are under way to incorporate QOL into
the radiation oncology clinic workflow directly.
Journal of the American College of Radiology
Berman et al n Personalized Medicine
AN EXAMPLE OF PERSONALIZED CARE FROM
SDM TO PATIENT-CENTERED RESEARCH:
EARLY-STAGE NON-SMALL-CELL LUNG
CARCINOMA
Lung cancer is the leading cause of cancer-related mortality. For patients with stage I non-small-cell lung carcinoma (NSCLC), the standard of care remains surgery
for those who are operable, and over the past decade,
stereotactic body RT (SBRT) has emerged as the highly
effective standard therapy for patients who cannot
tolerate or decline surgery [33].
Given its safety profile, and unexpected primary tumor control rates that exceed 90%, three phase 3 randomized studies were opened between 2008 and 2010 to
evaluate SBRT as an alternative to surgery in operable
patients. However, recruitment to these trials was challenging, as patients were commonly approached during
surgical consultations, which did not provide the optimal
equipoise between radiation and surgery if they were
labeled “medically operable.” Although each of these trials
was closed in 2013 because of poor accrual, a new generation of randomized studies currently seeks to recruit
patients to similar trials using modified strategies. These
include the STABLE-MATES (JoLT-Ca Sublobar
Resection [SR] Versus Stereotactic Ablative Radiotherapy
[SAbR] for Lung Cancer; ClinicalTrials.gov identifier
NCT02468024), SABRTooTH (A Study to Determine
the Feasibility and Acceptability of Conducting a Phase
III Randomised Controlled Trial Comparing Stereotactic
Ablative Radiotherapy With Surgery in Patients With
Peripheral Stage I Non-Small Cell Lung Cancer
Considered Higher Risk of Complications From Surgical
Resection; ClinicalTrials.gov identifier NCT02629458),
and VALOR (Veterans Affairs Lung Cancer Surgery or
Stereotactic Radiotherapy; Veterans Affairs Cooperative
Study Program 2005) studies. The recruitment schema
for STABLE-MATES (n ¼ 258) randomizes patients
before seeking consent in a process known as the Zelen
design, SABRTooTH (n ¼ 58) protects patients from
bias by limiting contact with surgeons and/or radiation
oncologists until pulmonologists can complete the consent and randomization process, and VALOR (n ¼ 670)
aims to safeguard patients from bias by educating patients
about two potentially equivalent treatment options before
a navigated consent process in which research associates
accompany patients during surgical and radiation
oncology consultations [34]. The success of each of these
trials will provide meaningful insights into the value of
SDM during recruitment to difficult randomized trials.
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However, the results of these trials may not be available
for many years to come.
The conundrum posed by a lack of completed randomized trials for this disease is highlighted by the results
of a pooled analysis of the prematurely closed ROSEL
(Trial of Either Surgery or Stereotactic Radiotherapy for
Early Stage [IA] Lung Cancer; ClinicalTrials.gov identifier NCT00687986) and STARS (Randomized Study to
Compare CyberKnife to Surgical Resection in Stage I
Non-Small Cell Lung Cancer; ClinicalTrials.gov identifier NCT00840749) trials that demonstrated a statistically significant 16% overall survival advantage with
SBRT at 3 years [35]. Although such a comparison was
underpowered (n ¼ 58 of 1,990 planned), the findings
are a likely contributor to an ongoing shift from surgery
to SBRT for early-stage NSCLC.
Clinicians may look to the literature to guide decisions, including studies that demonstrate no declines in
QOL after lung SBRT [36]. However, clinician
perceptions of the available data are variable, as recently
shown in a binary-choice experiment between SBRT
and surgery that revealed strong specialty biases, further
underscoring the importance of SDM [30].
Given the dilemma outlined here, a patient-centered
approach may be critical when counseling patients with
operable stage I NSCLC. This might be particularly
important if a goal is to minimize decisional regret, and
multiple organizations including the Patient-Centered
Outcomes Research Institute, have prioritized funding
SDM in both the screening and treatment of lung cancer.
At the University of Pennsylvania, efforts are underway
to develop and validate a personalized, web-based, electronic DA for patients with early-stage NSCLC choosing
between SBRT and surgery, and these data will be used in
a randomized trial with the primary end point of decisional conflict [37,38]. The secondary end points
incorporate additional patient-centered outcomes,
including QOL (VR-36), emotional distress (Impact of
Event Scale), and patient-centered communication.
Studies such as this will hopefully provide much needed
guidance for patients and clinicians whenever there is an
absence of high-level evidence for any disease when more
than one treatment option is available.
CONCLUSIONS AND FUTURE DIRECTIONS
The future will undoubtedly be defined by the various
stakeholders in patient-centered research in radiation
oncology. The critical and most evident beneficiary
of patient-centered research is the patient, whether
1576
incorporating a DA into the patient-physician conversation or incorporating PROs into critical, practicechanging trials. Patient advocacy groups, including the
NCI’s Advocate in Research Working Group, are
constantly supporting patient-centered research both in
the clinic and in investigations in radiation oncology [39].
Physicians and health systems are eager to incorporate
DAs into routine clinical care, the EHR, and consensus
clinical pathways, which have been shown to improve
consistent quality [14]. Educators are recognizing that
they must specifically train physicians in how to
approach an SDM model [40]. Moreover, physician
groups are equally engaged in pushing forward a
patient-centered research agenda; NRG Oncology has a
focused patient-centered outcomes research committee
that aims specifically to focus on these issues and the
American Society of Clinical Oncology’s Value Framework Project was recently revised to specifically call for a
patient-centered oncology model [41]. Last, insurers,
beyond starting to think about how to compensate
appropriately for high-quality, patient-centered care, are
considering how to specifically reimburse for the resources required to build DAs and participate in validated
SDM.
Personalized RT will be greatly enhanced with SDM
and PROs in the clinical and research setting; at the same
time, the field is also fortunately rife with other essential
aspects of “personalized” RT: molecular genomics that
may allow RT dose escalation or de-escalation, including
current successful ongoing de-escalation efforts in human
papillomavirus–positive head and neck cancer; real-time
adaptive radiation replanning, such as real-time imaging
with MRI or the ongoing RTOG 1106/ACRIN 6697
Randomized Phase II Trial of Individualized Adaptive
Radiotherapy Using During-Treatment FDG-PET/CT
and Modern Technology in Locally Advanced NSCLC,
investigating changing RT fields on the basis of functional PET images midway through treatment to allow
safer and more effective RT dose escalation. Moreover,
research is under way uniting QOL outcomes with the
underlying genetics at a molecular level in the establishment of the GeneQol Consortium, which is the ultimate
way of integrating “personalized” medicine at various
levels [42]. Taken together, the future of radiation
oncology will be highly specialized and based on
integrating the whole person and his or her molecular
fingerprint.
We are confident that our field, particularly through
the strong efforts of NRG Oncology, is focusing on
personalized medicine at multiple levels and helping
Journal of the American College of Radiology
Volume 13 n Number 12PB n December 2016
define the future of patient-centered care in radiation
oncology through SDM using DAs, validated metrics,
and driving PROs in the front seat, where they belong.
TAKE-HOME POINTS
-
-
-
-
-
SDM has been identified as a key element of
high-quality, patient-centered care and has been
associated with improved patient knowledge and
satisfaction, physical and emotional well-being, and
trust in providers.
In radiation oncology, growing attention has been
devoted to developing and systematically investigating patient DAs to aid patients in their treatment
choices.
QOL metrics significantly predict outcomes,
including local control and survival, and PROs are
increasingly being used in routine patient-physician
communication and incorporated as primary end
points in critical prospective trials.
SBRT for early-stage NSCLC has emerged as an
excellent alternative to surgery in selected situations, and the ongoing trials represent useful
examples of organized SDM and incorporation of
PROs.
NRG Oncology and its legacy cooperative groups
have been long-standing supporters of patientcentered outcomes and continue to drive forward
oncology trials using validated QOL data and
PROs.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
ADDITIONAL RESOURCES
Additional resources can be found online at: http://dx.
doi.org/10.1016/j.jacr.2016.09.012.
19.
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Journal of the American College of Radiology
Volume 13 n Number 12PB n December 2016