adult cancer survivorship: evolution, research, and planning ......childhood cancer survivors have...

DOI: 10.3322/caac.20040 2009;59;391-410 CA Cancer J Clin

Hampshire, Carolyn Vachani, Donna Pucci and Anna T. Meadows Joseph Carver, Clarisa Gracia, Christine E. Hill-Kayser, James M. Metz, Margaret K. Linda A. Jacobs, Steven C. Palmer, Lisa A. Schwartz, Angela DeMichele, Jun J. Mao,

Adult Cancer Survivorship: Evolution, Research, and Planning Care

This information is current as of August 6, 2010

http://caonline.amcancersoc.org/cgi/content/full/59/6/391located on the World Wide Web at:

The online version of this article, along with updated information and services, is

http://caonline.amcancersoc.org/subscriptions/individuals only): , go to (USCA: A Cancer Journal for CliniciansTo subscribe to the print issue of

Print ISSN: 0007-9235. Online ISSN: 1542-4863. Williams Street NW, Atlanta GA 30303. (©American Cancer Society, Inc.) All rights reserved.

is owned, published, and trademarked by the American Cancer Society, 250CANovember 1950. Society by Wiley-Blackwell. A bimonthly publication, it has been published continuously since

is published six times per year for the American CancerCA: A Cancer Journal for Clinicians

by on August 6, 2010 (©

Am

erican Cancer S

ociety, Inc.) caonline.am

cancersoc.orgD

ownloaded from

http://caonline.amcancersoc.org/cgi/content/full/59/6/391

http://caonline.amcancersoc.org/subscriptions/

http://caonline.amcancersoc.org:80

Adult Cancer Survivorship: Evolution, Research, andPlanning Care

Linda A. Jacobs, PhD, RN1; Steven C. Palmer, PhD2; Lisa A. Schwartz3; Angela DeMichele, MD, MSCE4; Jun J. Mao, MD, MSCE5;Joseph Carver, MD6; Clarisa Gracia, MD, MSCE7; Christine E. Hill-Kayser, MD8; James M. Metz, MD9;

Margaret K. Hampshire, BSN, RN10; Carolyn Vachani, MSN, RN11; Donna Pucci, MHK12; Anna T. Meadows, MD13

AbstractIncreases in the number of adult cancer survivors and other issues have forced the oncology community to examine,evaluate, and alter the cancer care paradigm. Pediatric oncologists are grappling with the task of transitioning agrowing population of adult survivors of childhood cancer to adult medicine, while oncologists caring for adultcancer survivors are seeking models of follow-up care that are acceptable to patients and providers. Workforce andaccess-to-care issues suggest that primary care providers will see more cancer survivors in their practices acrosstime, although it is unclear how prepared they are for this task. Translational research is needed to developevidence-based clinical care and survivorship care plans. A broad picture of the evolving field of adult cancersurvivorship is presented. The recent focus on young adult survivors of childhood cancer, an overview oftranslational research needed to inform the physical and psychosocial care of cancer survivors, and the roles ofprimary and specialty care providers managing this population is examined. Finally, an overview of evolvingtreatment summary and care plan initiatives is presented. CA Cancer J Clin 2009;59:391–410. ©2009 AmericanCancer Society, Inc.

To earn free CME credit or nursing contact hours for successfully completing the online quiz based on this article, goto http://CME.AmCancerSoc.org.

IntroductionConcern for cancer survivors and their long-term care developed initially as a result of significant improvementsin curing children and adolescents with cancer. During the last 3 decades, a population of young adult cancersurvivors has emerged, many with special needs that require ongoing care and surveillance. Some of thesechildhood cancer survivors have continued to receive follow-up care in pediatric oncology settings well intoadulthood, despite the fact that the likelihood of their primary cancer recurring is remote. At this phase of care,

1Director, LIVESTRONG Survivorship Center of Excellence, Abramson Cancer Center, University of Pennsylvania, Philadelphia, Pennsylvania, Clinical AssociateProfessor, University of Pennsylvania School of Nursing, Philadelphia, Pennsylvania; 2Research Assistant Professor, Department of Psychiatry, University ofPennsylvania School of Medicine, Philadelphia, Pennsylvania; 3The Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania; 4Associate Professor,Department of Medicine, Divisions of Hematology/Oncology and Epidemiology, Abramson Cancer Center, University of Pennsylvania School of Medicine,Philadelphia, Pennsylvania; 5Assistant Professor, Department of Family Medicine and Community Health, University of Pennsylvania School of Medicine,Philadelphia, Pennsylvania; 6Associate Professor, Department of Medicine, Penn Heart and Vascular Center, Chief of Staff, Abramson Cancer Center,University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania; 7Assistant Professor, Obstetrics and Gynecology, Department of ReproductiveEndocrinology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania. 8Chief Resident, Department of Radiation and Oncology, Universityof Pennsylvania School of Medicine, Philadelphia, Pennsylvania; 9Associate Professor and Vice Chair, Department of Radiation Oncology, University ofPennsylvania School of Medicine, Abramson Cancer Center, University of Pennsylvania, Philadelphia, Pennsylvania; 10Oncology Nurse, Department ofRadiation Oncology, Managing Editor OncoLink, Abramson Cancer Center, University of Pennsylvania, Philadelphia, Pennsylvania; 11OncoLink Nurse Educator,Abramson Cancer Center, University of Pennsylvania, Philadelphia, Pennsylvania; 12Research Coordinator, LIVESTRONG Survivorship Center of Excellence,Abramson Cancer Center, University of Pennsylvania, Philadelphia, Pennsylvania; 13Professor, Department of Medicine and Pediatrics, The Children’s Hospitalof Philadelphia, University of Pennsylvania School of Medicine, Abramson Cancer Center University of Pennsylvania, Philadelphia, Pennsylvania

Corresponding author: Linda Jacobs, LIVESTRONG Survivorship Center of Excellence Abramson Cancer Center, University of Pennsylvania School of Medicine, Philadelphia,Pennsylvania 19104. [email protected]

DISCLOSURES: Financial support for this study was provided by the Lance Armstrong Foundation, the Sarah Rosato Fund, the VanBuren Family Fund, the Alison andRichard Prezelski Fund, and the American Cancer Society (CCCDA-08-107-08).

�2009 American Cancer Society, Inc. doi:10.3322/caac.20040.

Available online at http://cajournal.org and http://cacancerjournal.org

CA CANCER J CLIN 2009;59:391–410

391VOLUME 59 � NUMBER 6 � NOVEMBER/DECEMBER 2009


Am

erican Cancer S


cancersoc.orgD

ownloaded from


the focus for them, as well as for the much largernumber of survivors of adult cancers, turns to sur-veillance for and management of long-term and lateeffects that occur as a result of cancer and its treat-ment, as well as routine health promotion and pre-vention of disease.

More than 40% of people born today in the UnitedStates will be diagnosed with cancer at some point intheir lives.1 Advances in screening and treatmenthave contributed to lengthening the survival periodfor many of these individuals, and long-term survivalis now a possibility for many patients. The need forcancer care to more fully address survivorship issueshas been the subject of numerous conferences, work-shops, and symposia sponsored by such groups as theNational Cancer Institute (NCI), the National Co-alition for Cancer Survivorship (NCCS), and mostrecently, the Institute of Medicine (IOM). TheNCCS, founded in 1986, was responsible for addingthe term “survivorship” to cancer care2,3 and forheightening awareness of the importance of lookingbeyond cancer treatment to the survivorship phase ofcare. However, the adult oncology community hasbeen slow to embrace the notion that this phasewarrants significant and separate attention.

In 1997, the Lance Armstrong Foundation wasfounded and with additional support from influ-ential groups such as the NCI and the AmericanCancer Society (ACS) has contributed to bringingsurvivorship to the forefront of the oncology com-munity.4 In 2006, a committee established by theIOM published a seminal report, From CancerPatient to Cancer Survivor: Lost in Transition,which examined a broad range of medical andpsychosocial issues faced by cancer survivors as aconsequence of their diagnosis and its treatment

and has probably been most responsible for draw-ing attention to the survivorship phase of care.2

The IOM report identified cancer survivorship asa distinct phase of care that has been neglected inareas such as advocacy, education, clinical practice,and research. The report recognized 4 essential com-ponents of patient-centered survivorship care (Table1), and 10 recommendations for improving the careprovided to survivors were made (Table 2).2 Theserecommendations are far-reaching and broad, requir-ing cooperation among health care providers, re-searchers, advocacy groups, professional organiza-tions, government bodies, and policy makers. Since2006, there have been numerous publications outlin-ing and discussing the report, with many focusing onthe recommendation that patients completing pri-mary cancer treatment “be provided with a compre-hensive summary of their treatment together with a

TABLE 1. Essential Components of Survivorship Care

ESSENTIAL COMPONENTS OF SURVIVORSHIP CARE

1 Prevention of recurrent and new cancers, and other late effects

2 Surveillance for cancer spread, recurrence, or second cancers;assessment of medical and psychosocial late effects

3 Intervention for consequences of cancer and its treatment

4 Coordination between specialists and primary care providers toensure that all of the survivor’s health needs are met

Hewitt M, Greenfield S, Stovall E, eds. From Cancer Patient to Cancer Survivor: Lost in Transition. Washington, DC: National Academies Press; 2006.

TABLE 2. IOM Recommendations for Survivorship Care

RECOMMENDATIONS FOR SURVIVORSHIP CARE

1 Raise awareness of cancer survivorship

2 Provide a care plan for survivors

3 Develop clinical practice guidelines for cancer survivors

4 Define quality health care for cancer survivors

5 Overcome health care system challenges

6 Address survivorship as a public health concern

7 Provide survivorship education and training of health careprofessionals

8 Address employment concerns of cancer survivors of all ages

9 Improve access to adequate and affordable health insurance

10 Invest in research

IOM indicates Institute of Medicine.

Hewitt M, Greenfield S, Stovall E, eds. From Cancer Patient to Cancer Survivor:Lost in Transition. Washington, DC: National Academies Press; 2006.

Adult Cancer Survivorship

392 CA: A Cancer Journal for Clinicians


Am

erican Cancer S


cancersoc.orgD

ownloaded from


survivorship follow-up care plan written by the treat-ing health care provider(s).”2

This is a challenging task for reasons that includeworkforce and reimbursement issues and a lack ofempirical guidelines on which to base recommenda-tions and develop survivorship care plans. Pediatriconcology has taken the lead in developing treatmentsummaries and guidelines for follow-up care plans forpatients and their families and in communicating thisinformation to other health care providers. Theseguidelines have been written and managed by theChildren’s Oncology Group (COG).5 Although gen-erally consensus-based rather than data-driven, theserecommendations provide consistency for follow-upcare of childhood cancer survivors, a feature lackingin long-term follow-up care provided to adult cancersurvivors. There has been considerable debate abouthow to approach the development of survivorshipcare plans for adult cancer survivors. The IOM reportacknowledged that survivorship plans “have strongface validity and can reasonably be assumed to im-prove care unless and until evidence accumulates tothe contrary.”2 However, the adult oncology commu-nity has been hesitant to make consensus-driven rec-ommendations for follow-up care of adult cancersurvivors.

Oncology workforce issues are another factor to beconsidered when examining the broad topic of adultcancer-survivorship care delivery. The IOM exam-ined the workforce issue in the recent Ensuring Qual-ity Cancer Care through the Oncology Workforce: Sus-taining Care in the 21st Century workshop andpublication.6 They noted that the current crisis in thecancer-care workforce will worsen because of theaging and retiring of health care providers in oncol-ogy and primary care and because of the increasingnumber of cancer survivors. The long-term follow-upcare needs of cancer survivors combined with theincreasing focus on health promotion will further taxthe resources of available oncology practitioners andplace new and significant demands on primary careproviders who do not feel adequately prepared to carefor cancer survivors.6-13 Yet, as survivors increase andthe oncology workforce diminishes, primary and spe-cialty care practices will be caring for more long-termcancer survivors, and these cancer-care providersmust be prepared to do so.

Treatment summaries and survivorship care plansserve as effective communication tools between on-

cology practitioners and primary care physicians, andthese tools improve the confidence with which non-oncological physicians practice. They provide a focusfor the evolving field of adult survivorship that in-cludes clinical care, research, and education. Survi-vorship care plans engage survivors and cancer-careproviders alike and help to guide clinicians in theirclinical care of cancer survivors. Although data-driven surveillance guidelines have not been estab-lished for most adult cancers, clinically derived andconsensus recommendations are arising from a vari-ety of sources. As models are developing for the careof adult cancer survivors, thoughtfully designed eval-uative research must be conducted that can trulyinform clinical care and guide evolving models ofcare.

This article explores the emerging field of adultcancer survivorship. It is not easy to change a para-digm in which providers have historically focused oncancer treatment and cure. The field of adult cancersurvivorship is growing and demands are beingplaced on providers who lack adequate training, data,or practice standards to guide care for a rapidly grow-ing number of patients. As mentioned earlier, manyarticles have been published that outline the IOMrecommendations, the essential components of care,and the barriers to providing that care, includingoncology and primary care workforce issues.2,14-16 Inaddition, professional and advocacy groups have fo-cused on the need for and development of care plansfor cancer survivors despite a paucity of survivorshipresearch.18 We will attempt to bring these issuestogether, providing the reader with a broad picture ofthe evolving field of adult cancer survivorship. Theongoing work in the field of pediatric cancer survi-vorship care will be presented including the morerecent focus on the population of survivors of pedi-atric cancer who are now adults. Adult cancer-survi-vorship issues, including the what, why, and how oftranslational research that will inform the physicaland psychological care of this population, and theroles of primary care and specialty practitioners whoare caring for adult survivors at a time when there aresignificant workforce issues in oncological and pri-mary care will also be examined. Finally, we willpresent an overview of available treatment-summaryand care-plan templates, an in-depth view of a pa-tient-focused Internet-based treatment summary,and a care-plan initiative that has an integrated re-




Am

erican Cancer S


cancersoc.orgD

ownloaded from


search component driving the evolution of the prod-uct. Examination of these topics will provide thereader with a picture of the multifaceted scope of thechallenges faced by clinicians, researchers, adminis-trators, and adult cancer survivors themselves.

Pediatric Oncology Survivorship CarePrompted by IOM reports, medical oncologists, sur-geons, radiation oncologists, and other oncology careproviders now recognize that cancer survivors whohave completed therapy and have no evidence ofdisease are, nevertheless, at risk for problems that arelikely to reduce the quality and length of their sur-vival.2,18-21 Focus on survivorship care began withpediatric oncology in the 1970s as clinical trials wereprolonging the lives of more and more children withcancer. It was noted that normal tissues of growingchildren were especially likely to suffer from thedeleterious effects of radiation therapy and certainchemotherapeutic agents, and studies of selected co-horts of survivors continued into the decades of the1980s and 1990s.21-31 This led to the recognition thatsecond cancers, cardiac disease, neurocognitive dys-function, infertility, and other late complicationscould be attributed to specific therapies.22-24,32 Stud-ies of the late effects of treatment led to clinical trialsthat tested the efficacy of reducing the offendingagent(s) and also led to the elimination or reductionin dose of radiation for Wilms tumor, lymphomas,acute lymphocytic leukemia, and brain tumors.33-35

It was during the 1990s that the relation betweendose and outcome began to be studied, and effortswere made to inform survivors of their futurerisks.36-40 These initial reports of late effects in child-hood cancer survivors came from single institutionsor from multicenter consortia. In 1994, with fundingfrom the NCI, a multicenter cohort of long-termsurvivors of childhood cancer was assembled to ad-dress and overcome the limitations of earlier studiesthat had fewer subjects and shorter follow-up.41 TheChildhood Cancer Survivor Study (CCSS) publishedthe many aspects of survival in 14,000 children andadolescents who were characterized demographicallyby treatment from 1970 to 1986 and who survived forat least 5 years after diagnosis.42-45 As treatmentsevolved during the subsequent decades, the CCSSembarked on studies of children diagnosed from1987 to 1999 by using the same eligibility criteria and

seeking to address changes in quality of survival andlong-term and late complications.41

Caring for children who are likely to be cured ofcancer (approximately 90% of those who survive for 5years from diagnosis are in that group) involves un-derstanding that many of the late effects of therapydo not become apparent until childhood cancer sur-vivors are no longer a part of the pediatric follow-upsystem. The expertise of any one or more of thefollowing specialists is often necessary to address latecomplications: cardiologist, pulmonologist, gynecol-ogist, neurologist, or gastroenterologist. This needfor specialists to address the myriad of late effectsassociated with cancer treatments led to the emer-gence of long-term follow-up clinics where manyspecialists are available to returning survivors. Ratherthan monitoring for a recurrence of the original can-cer, these programs are designed to educate andcounsel survivors on the treatment they received andtheir potential late effects. They also serve as wellnesscenters, where recommendations for healthy lifepractices can be reinforced and referrals can be madeto appropriate specialists for the management of is-sues related to treatment.

How institutions provide appropriate follow-upcare for these survivors of childhood cancer has al-ways been a question. In 1999, to address this need,and by using the expertise available in the COG,guidelines for follow-up based on therapy were de-veloped; the third revision is online and may beaccessed by providers and survivors (http://www.sur-vivorshipguidelines.org).5 Despite the availability ofthese guidelines and the increasing number of spe-cialized clinics, it is estimated that fewer than 30% ofsurvivors 20 years from diagnosis return for follow-upcare, and many do not receive appropriate surveil-lance.5,46,47

Children and adolescents who survive cancer growinto adulthood and then require care that focuses ontheir needs as adults. Many childhood cancer survi-vors are lost to follow-up care as they mature, leavethe oversight of their parents, and take responsibilityfor their own medical care. As young adults, theyseek care on an “as-needed” basis and, for some ofthem, their providers pay little clinical attention totheir history of cancer and to the potential risks theseyoung adults face as a consequence of their previoustreatment.48-52




Am

erican Cancer S


cancersoc.orgD

ownloaded from


For this population of survivors, there is a criticalneed to address the following questions: How canthat majority of survivors of childhood cancers whohave been lost to risk-based follow-up be identifiedand recovered? How can we identify those adoles-cents and young adults who are ready to manage theircare in an adult setting? How can the COG guide-lines be adapted to provide guidance for the care ofadult survivors of childhood cancer? What is the bestway to transmit information to survivors and theirproviders? What is the best venue for follow-up careof adult survivors of childhood cancer? How can weevaluate whether our counseling and surveillancehave been effective in preventing or ameliorating lateeffects that are of significant concern for this group ofsurvivors?49,53

There are many obstacles to achieving a timely andsmooth transition from pediatrics to adult-focusedcare.48-52,54 Patients and families are sometimes re-luctant to leave institutions and caregivers in whomthey have confidence and with whom they have de-veloped a dependent relationship. Pediatric caregiv-ers are reluctant to relinquish the satisfaction thatcomes from seeing young adult patients who haveovercome cancer. Survivors themselves are often notconfident that they can manage their own care be-cause many report that they are often unable to recallinformation on the treatment they received that isnecessary to inform other caregivers and guide theircare.49-53 In addition, there are too few caregivers ofadults who are confident and capable of understand-ing the needs of survivors treated for cancer as chil-dren; consequently, many young adult survivors re-ceive less than optimal care.55 When treatmentintensity is limited and not complex, referrals canconfidently be made to primary and/or specialty careproviders.56 However, in the case of survivors whosetreatment involved multiple modalities and who havemany potential or actual late complications, a spe-cialized program designed for young adult survivorscan provide support for managing and possibly tran-sitioning the care of these patients to nononcologicalproviders.

Pediatric cancer centers across the country have de-veloped programs that deliver care to pediatric cancersurvivors, and many of these programs include youngadult survivors in the populations they follow. Theseprograms are based in pediatric settings, and survivorsare followed by providers focused on care within a

designated survivorship or late-effects clinic. These pro-grams provide ongoing care to pediatric cancer survi-vors, and some of these programs, when appropriateand/or at a certain age, refer young adult survivorsback to the community to be followed by adult on-cology specialty and/or primary care providers. Anexcellent example of this is the St. Jude After Com-pletion of Therapy (ACT) Clinic. This program isdesigned to assist young adults in transitioning theirfollow-up care to outside providers, as well as toprovide survivors and their families with informationand access to a wide array of services available in theircommunities. A comprehensive list of pediatric pro-grams that care for children after completion of treat-ment, including St. Jude’s, can be found on the Ped-Onc Resource Center Web site (http://www.acor.org/ped-onc/treatment/surclinics.html).

Given the relatively new focus on survivorshipwithin the adult oncology community, it is not sur-prising that adult oncology has not been quick toestablish a mechanism for providing care that wouldaddress the unique needs of adult survivors of child-hood cancer within an adult cancer care setting. TheTransition Program at the Abramson Cancer Center(ACC) of the University of Pennsylvania, establishedby Anna Meadows, MD, in 2002 as a collaborativeeffort between The Children’s Hospital of Philadel-phia (CHOP) and the ACC, is one of the fewprograms in the country that is based in an adultcancer care setting. This program focuses on transi-tioning young adult survivors of childhood cancer toan adult medical setting where appropriate risk-basedfollow-up care can be provided. The family and sur-vivor receive considerable support during the transi-tion process in order to attenuate the difficulties thatcan arise when survivors move from the protectiveenvironment of a pediatric setting to what is per-ceived as the more difficult-to-navigate world ofadult care. The Dana Farber Cancer Institute, theUniversity of Colorado Cancer Center, and the Uni-versity of California at Los Angeles are examples ofother institutions that have recently developed simi-lar programs in adult oncology (personal communi-cations).

Caring for Adult Cancer SurvivorsThe number of adult cancer survivors in the UnitedStates has grown to approximately 12 million57 and is




Am

erican Cancer S


cancersoc.orgD

ownloaded from


likely to double by 2050.58 Survivorship follow-upcare is an essential component of cancer care.17 Can-cer can represent a “teachable moment” for manyindividuals,59 and behavioral modifications, psychos-ocial adjustments, detection of late effects, and man-agement constitute important issues in follow-upcare.2,17,59,60 However, research necessary to under-stand and frame these concerns and to structure aplan of care for adult cancer survivors has not beenadequate, and follow-up recommendations have beenbased primarily on consensus in the absence of LevelI evidence.61 In recognition of this phenomenon,both the National Institutes of Health Office ofCancer Survivorship and philanthropic groups, suchas the Lance Armstrong Foundation, have supportedresearch initiatives in cancer survivorship that hopeto provide evidence that will guide the care andfollow-up of adult cancer survivors. Such researchspans many areas, including behavioral, health ser-vice, and translational investigation.

Translational Research to InformClinical Survivorship CareTranslational survivorship research is key to under-standing the specific risks and late effects for indi-viduals who have developed and been treated forcancer. For example, what is the incidence of cardiacdysfunction after anthracycline-based chemotherapy,and who is at risk? What is the risk of a secondprimary cancer after radiation to the chest? What arethe fertility issues faced by the large cohort of adultsurvivors treated as children as well as young adultsdiagnosed and treated in their childbearing years?Does the provision of care for survivors by oncology,primary care, and specialty care providers influencethe uptake of health-promoting behaviors amongcancer survivors? Such questions are at the heart ofpersonalized cancer care.

More questions are likely to arise as more patientssurvive for longer periods following chemotherapyand radiation. Large patient cohorts or case-controlapproaches are necessary to accurately estimate inci-dence or prevalence rates and to evaluate multiplerisk factors for developing late and long-term effects.The use of databases linked to cancer outcomes, suchas the SEER-Medicare linked databases, is one ap-proach to a research design. However, this approachhas limitations, including findings that most patients

in the database are older than age 65 years and thatdetailed treatment information or outpatient thera-pies are not well characterized. Claims databases maynot be accurate in capturing all outcomes of interestapart from the primary event that led to hospitaliza-tion. Thus, there is a need for coordinated efforts toassemble large patient cohorts that are well annotatedand have long follow-up histories. Ongoing clinicalcare for cancer survivors is crucial to the collection ofinformation on subsequent lifestyle, medication, andother exposures, as well as the development of secondcancers and other medical conditions over time.

Another challenge to translational research is that,as oncologists who treat adults learned from theircolleagues who treat pediatric patients, outcomes ofinterest often occur years to decades from the time ofexposure to treatment. Thus, development of surro-gate biomarkers is essential to identifying patients atrisk and for monitoring development of late effects.Such biomarkers would ideally provide the opportu-nity to identify susceptible patients at a time wheninterventions can be most effective at preventing orameliorating late effects. These markers can also pro-vide an opportunity for screening. Important surro-gate markers of processes, such as late pulmonary,cardiac, hepatic, or renal effects, require collection ofserum or urine.62 Genetic markers require the collec-tion of blood for polymorphonucleic cells, cheekswabs, or other sources of germline DNA. Collectionof tumor, premalignant, and normal tissue at thetime of diagnosis can provide important resources forresearch on cancer susceptibility, the development ofsecond cancers, and strategies for intervening at apremalignant stage. Optimally, biological specimensshould be collected at diagnosis as well as periodicallyover the course of follow-up. Specimen banks thatuse standardized collection procedures are essentialto the forward movement of the field of cancer sur-vivorship practice, as the development of assays andplatforms advance over time and new hypotheses aredeveloped.

One area in which research has been performed isthe area of second cancers. Second cancers accountfor a significant proportion of new cancers diagnosedannually and can reflect late effects of treatment,influence of lifestyle, environmental exposures, hostfactors, and combinations of influences that includegene-environment and gene-gene interactions. In2004, the NCI hosted a workshop entitled, Cancer




Am

erican Cancer S


cancersoc.orgD

ownloaded from


Survivorship: Genetic Susceptibility and Second Pri-mary Cancers.63 This conference brought together amultinational group of experts on epidemiology, on-cology, and survivorship research to address “researchissues, priorities, resources, and infrastructure re-quirements needed to advance the field.”63 Key rec-ommendations included the development of researchinfrastructure for studies of cancer survivorship, in-cluding multicenter adult cancer survivor cohortsculled from individual treatment centers; clinical trialcooperative groups; population-based cancer regis-tries; a coordinated system of biological specimencollection; development of new technology, biomar-kers, and bioinformatics; and development of newepidemiological study designs and methods. Al-though these recommendations were formulatedwith the goal of expanding and facilitating researchon second cancers, they are critical components nec-essary to all translational research in cancer survivor-ship.

Health Behavior Research to InformClinical Survivorship CareAs cancer has become as much a chronic healthcondition as an acute health crisis, it is imperativethat care of survivors and research focus on psycho-social as well as physiological consequences of cancertreatment. Much behavioral research to date has em-phasized psychological and social sequela of cancersurvivorship. This research has focused on issues suchas emotional distress and psychiatric disturbance, in-formational and knowledge needs, and more biolog-ical-behavioral areas such as fatigue, pain, and cog-nitive-impairment complaints. Social concerns suchas finances, employment, and insurance have alsobeen examined. These areas of clinical research havebeen well-described in a recent IOM report, CancerCare for the Whole Patient: Meeting Psychosocial HealthNeeds, which outlines psychosocial concerns amongcancer survivors and provides models of care andrecommendations for addressing these.64 Although athorough recapitulation of this report is beyond thescope of the present article, it is worth noting that thereport described a set of 5 components common toeffective intervention programs (Table 3).

An area of research that has received less attentionconcerns health behaviors practiced by cancer survivors,including behaviors that enhance their quality of life,

seeking screening for new and secondary malignancies,and pursuing reduction of late effects of treatment. Thisis especially important given the aging population ofadult cancer survivors whose health is disproportion-ately impaired by normal aging processes.65 Althoughhealth-promoting behaviors are important for thehealth of any individual, they are even more crucialamong cancer survivors given the potential for treat-ment that leads to organ dysfunction, tissue damage,and future morbidities.66 Engagement in health-pro-moting behaviors such as cancer screening, sun safety,nutritional intake, exercise, and avoidance of smoking,drugs, and alcohol may minimize the risk of manypoor-health outcomes.

Unfortunately, little is known about how the ex-perience of survivorship and risk-based care influenceuse of preventative services. Furthermore, the pro-cesses leading survivors to engage in health-promot-ing or risk-avoidance behaviors are not well under-stood. These issues are important as long-termcancer survivors report poorer health and greater roleinterference than matched controls; these effects areamplified by the presence of chronic comorbidities.67

An overview of findings from both single-institutionand large-scale epidemiological studies is presentedalong with limitations and suggestions for futuredirections.

Health Behavior Research in AdultSurvivors of Childhood CancersAs summarized by Clarke and Eiser,68 survivors ofchildhood cancers engage in health-risk behaviors at thesame or lower rates as comparison groups. Although

TABLE 3. Essential Components of PsychosocialSurvivorship Care

ESSENTIAL COMPONENTS OF PSYCHOSOCIAL SURVIVORSHIPCARE

1 Identify psychosocial difficulties and develop care plans withpatients.

2 Connect patients with appropriate services.

3 Support patients in managing their illnesses.

4 Coordinate psychosocial and biomedical care.

5 Provide follow-up assessment to monitor and evaluate outcomesand to make appropriate alterations in care plans.

Adler N, Page A, eds. Cancer Care For The Whole Patient: Meeting PsychosocialHealth Needs. Washington, DC: The National Academies Press; 2008.




Am

erican Cancer S


cancersoc.orgD

ownloaded from


not worse than the general population, these rates aresomewhat concerning based on survivors’ increased riskfor new cancer diagnoses (30-year cumulative risk forsecond neoplasm is 9.3%)20 and other health problems(62.3% have at least 1 chronic condition).51 For exam-ple, whereas rates of smoking among childhood cancersurvivors are generally found to be the same or less thanthe general population, any smoking is too much givenits exacerbation of already existing risk for cardiac andpulmonary disease and second cancers.66 Survivors arealso less likely to meet recommendations for physicalactivity, and they report engaging in fewer leisure ac-tivities than their siblings.69 Demark-Wahnefried et al70

reported that only 21% of a sample of 200 adolescentand young-adult survivors met guidelines for fruit andvegetable consumption, 32% met guidelines for calciumintake, 48% met guidelines for exercise, and 42% wereoverweight or obese. These findings are similar to thosereported in the Youth Risk Behavior Surveillance(YRBS) survey71 concerning guideline-congruent fruitand vegetable consumption (21.4%) and slightly belowthe proportion of those aged 19-30 years in the Na-tional Health Interview Survey (NHIS) who are ex-ceeding calcium-intake guidelines (38.8%).72 However,they reflect a much higher rate of obesity and over-weight status than reported in the YRBS (28.8%), likelyresulting, at least in part, from decreased physical activ-ity seen among adolescent and young adult (AYA)cancer survivors.73,74

Screening practices, as well, fall below optimal levelsfor survivors of childhood cancers. Yeazel73 reportedthat although survivors tended to perform screeningbehaviors at a higher rate than siblings, only 28% offemales regularly performed breast self-examination,and only 17% of males performed testicular self-examinations. Although 80% of females had received aPap smear within the previous 3 years, and 62% hadhad a clinical breast exam, only 21% had received amammogram. Receipt of mammography was higher(57%) among those women at highest risk (older thanage 30 years and those who had received chest or mantleradiation) but remains less than optimal. Similarly,among women who received chest radiation, 64% ofthose ages 25-39 and 24% of those ages 40-50 had notreceived screening mammography within the previous 2years, despite guidelines that these women should re-ceive annual mammograms.74

Such health behaviors may be deemed suboptimalon the basis of lack of survivor awareness of their

risks and lack of risk-based follow-up care.66 More-over, differences exist in how health-risk manage-ment behaviors among survivors of childhood cancerare acquired and maintained compared with theirpeers. This is exemplified by findings that suggestthat survivors who smoke are less likely to attempt orto successfully quit smoking75 and by findings thatpsychological sequela of cancer, such as post-trau-matic stress, depression, and worries about illness,relate to poor health behaviors.32,76-79

Behavioral Research in Survivors ofAdult Onset CancersA few large-scale studies of the preventative andhealth behaviors of adult cancer survivors have nowbeen published. In a study of more than 9000 cancersurvivors, Blanchard et al80 reported that these sur-vivors comprised 6 different tumor locations and that8.4% to 17.4% were current smokers, which is on thelow end and may reflect absence of survivors of lung,head and neck, and other cancers in which smokingis more prevalent. Large population-based studiesfrom the United States and Australia67,81,82 have es-timated the rate of smoking among survivors to be atleast 20%. Of particular importance to providers ofcare to cancer survivors is a consistent finding thatyoung adult cancer survivors are smoking at a rateabove that of their comparison groups67,81 with ratesamong those survivors younger than age 40 years ashigh as 38% according to NIHS data.83 Alcohol useappears common in this population as well, withCoups and Ostroff83 and Bellizzi et al81 reportingmoderate to heavy use by 15% to 16% of cancersurvivors. This is not substantially different fromnoncancer controls.

Rates of self-reported dietary adherence and phys-ical activity are also less than ideal. Coups and Os-troff83 found that across age-stratified survivorgroups, at least 45% were meeting 5-a-day recom-mendations for fruit and vegetable consumption.Similarly, adherence to physical activity recommen-dations ranged from 30% to 52% of survivors.80-83

Not surprisingly, this is reflected in rates of body-mass-index–determined categories of overweightand/or obese survivors that range from 52% to 69%,although again, these rates for survivors are not sub-stantially different from those in the general popula-tion. Survivors appear to be meeting recommenda-




Am

erican Cancer S


cancersoc.orgD

ownloaded from


tions for surveillance and screening, and, overall, arereporting adherence rates that are at least as high asnoncancer controls. By using NHIS data, we findthat 99% of female survivors appear to have ever hada Pap smear, and more than three-fourths are cur-rently meeting screening recommendations.81,84,85

Mammography recommendations are met by 75% to88%, with 92% reporting ever having had a mammo-gram. Similarly, between 56% and 76% of survivorsfor whom prostate-specific antigen tests are discussedhave had them performed. Although these data arepromising, it should be remembered that they arebased on self-reports of health behaviors rather thanon examination of medical records, and, therefore,may be somewhat biased toward adherence to posi-tive behaviors and denial of risk behaviors.

Next Steps in Advancing the Field ofAdult Cancer Survivorship CareUntil recently, studies that examine health behaviorsamong adult cancer survivors have been predomi-nantly small, cross-sectional, or retrospective, andfrom single institutions and primarily tertiary-carecancer centers. Additionally, the focus, more oftenthan not, has been on short-term (ie, less than 5years) breast cancer survivors. Consequently, much ofthis work has been performed with selected groups ofpatients who may or may not represent all survivorsin these settings. More recent population or largedata-based studies have emerged, such as the CCSSand the NHIS, and data are accumulating from theAmerican Cancer Society’s Studies of Cancer Survi-vors.4 These studies have described prevalence ofhealth behaviors among survivors and have identifieda need for prevention and intervention to enhancehealth outcomes for survivors. However, significantshortcomings include reliance on self-reports of bothcancer history and health behaviors with brief, not-validated indices and a lack of well-described anddocumented treatment exposures.

For example, the NHIS has been used numeroustimes to gather data on survivors but is not specifi-cally designed to assess cancer-related variables. Inthe NHIS survey, cancer history and health behaviorsare self-reported, important contextual information(eg, prevalence of referrals, use of behavioral sup-ports) is absent, and sampling does not representsurvivors-at-large. In particular, although adults

older than age 65 years represent more than 62% ofcurrent cancer survivors, this age group is seldomadequately represented. Furthermore, those who re-side in institutional settings and, thus, may be ex-pected to have the greatest morbidity burden are notrepresented at all in the NHIS. In addition, thesedata remain cross-sectional and retrospective, allow-ing little insight into changes that occur in healthbehaviors across the cancer trajectory. Our under-standing of health behaviors and how they changeover time will be greatly enhanced with better doc-umentation from physicians and access to medicaldatabases that capture comparable data and allowmulti-institutional data to be linked to larger net-works. In addition, providing mechanisms and fund-ing opportunities for follow-up of clinical trial par-ticipants would allow for long-term survivorship datato be collected on very well-characterized samples.

Adoption of recommendations such as those madeby the President’s Cancer Panel 2005-200686 that allclinical trials collect psychological risk-factor datacould do much to advance our understanding ofpredictors of adaptation and to allow early identifi-cation of those at risk for long-term difficulties. Un-fortunately, the rate of participation of adult cancerpatients in clinical trials is low and selective. Forexample, it was recently estimated that only 1.7% ofthe incident cases of breast, colorectal, lung, or pros-tate cancer were enrolled onto NCI CooperativeGroup trials, with significantly lower accrual amongAfrican Americans, Hispanics, and the elderly.87 Ab-solute numbers of participants, however, is highenough for very meaningful data to be generated bysuch an endeavor. Additionally, research across thespectrum needs to include improvements in measure-ment that provide standardized assessments of healthbehaviors and linkages to quality-of-life and objectivehealth outcomes.

Acknowledging deficiencies in research that exam-ines cancer-related health behaviors may be consid-ered a first step toward developing care plans withsurveillance recommendations for which efficacy andcompliance have been tested. Although interventionprojects have been developed, they have not beenwidely disseminated beyond academic medical cen-ters. This process is complicated by the finding thatmany patients transition their care from a tertiarycenter to geographically more accessible centers orprimary care providers who are better able to meet




Am

erican Cancer S


cancersoc.orgD

ownloaded from


their long-term needs. Thus, interventions to im-prove the health behaviors of survivors must be ableto be generalized to a range of settings, able to beimplemented by various health care providers, andwilling to take patient preferences into account.

Despite inroads made into the fields of, mainly,pediatric cancer survivorship, research, and care, ev-idence-based surveillance guidelines are not availableto guide the care of any adult cancer survivors, in-cluding young adult survivors of childhood cancers,and considerable research is still needed as this pop-ulation ages. Research in this population will likelyprovide data and recommendations for comprehen-sive clinical care of adult cancer survivors of all ages.

Clinical Care Providers for Adult CancerSurvivorsA shortage of oncologists recently reported by theAmerican Society of Clinical Oncology (ASCO)88 isoccurring at the same time as the demand for oncol-ogy services is expected to rise. This will require thatoncologists work with primary care providers to playa major role in caring for survivors across the cancertrajectory. However, the shortage and inadequatepreparation of primary care physicians to address thecomplex concerns of cancer survivors are also well-documented.10,11,14,15,89,90 These issues pose a con-cern to the oncology community.2,6

Whereas a significant number of cancer survivorscontinue to receive cancer follow-up care from on-cologists in the United States, many are cared for byprimary care and other specialty care providers.91 In astudy among breast cancer survivors aged 65 years orolder, only 27% of survivors saw their oncologistsannually for 3 years following active treatment.92

These survivors have more health care encounterswith their primary care providers than with theironcologists.10,11,14,15,89,90 In addition, as cancer survi-vors age, they face managing late effects of cancertherapies (eg, accelerated cardiovascular-, pulmo-nary-, and bone-health decline),93 as well as otherongoing comorbid illnesses (eg, diabetes, arthritis,recurring pain, and distress).94 The complexity of thehealth issues faced by survivors requires coordinated,patient-centered care and a paradigm shift from dis-ease-focused to wellness-centered comprehensivecare. Survivorship care focuses on restoring healthand preventing recurrence; therefore, care of cancer

survivors needs to be personalized, preventative, andparticipatory. Thus, an essential component of healthcare for cancer survivors is active involvement ofprimary and specialty care providers.95

Traditionally the role of primary care providers incancer control was screening and prevention. How-ever, because the overall 5-year survival rate for can-cer now exceeds 65%, many cancer survivors return totheir primary care providers for follow-up and rou-tine care, and some see their primary care providerexclusively for cancer and other follow-up care.96

Studies suggest that primary care providers are morewilling to participate in the care of survivors96,97 thanhas been perceived by survivors and oncologists. Al-though adequate resources, communication amongproviders, and access to information have been iden-tified as important in the care of survivors,96 primarycare providers have identified poor communicationwith the oncology team as a factor making transitionof care more difficult.97 Inadequate knowledge ofcancer care and treatments have also been identifiedas barriers for nononcology providers7,96 as has thecurrent workload of primary care providers.96 Pa-tients have reported that although they endorse theirprimary care providers’ ability to provide general care,they had concerns about these providers’ ability toprovide survivorship-specific care.10

Studies that used large administrative databaseshave noted that older survivors followed by primarycare tend to receive inadequate screening for cancerrecurrence, although they receive comprehensive pre-ventative services, including screening for other can-cers.10,98-100 Survivors who received care from on-cologists tended to receive cancer-specific follow-upbut fewer preventative health services, whereas thosewho received care from both received cancer-specificand other preventative health services.91,101 Recentclinical trials suggest that with education and a treat-ment algorithm, primary care providers can delivercare similar to that of oncologists with respect tocancer-recurrence detection for breast and colorectalcancers.102,103

The care of survivors needs to be negotiatedamong providers and the patient, and one size prob-ably won’t and shouldn’t fit all when it comes todeveloping a plan for post-treatment care. Patientsoften build strong relationships with their oncologyteam and, in many cases, use the oncology team forprimary health care. Survivors may view their oncol-




Am

erican Cancer S


cancersoc.orgD

ownloaded from


ogist as the one who saved their life and, conse-quently, trust only the oncology team with the com-prehensive management of their care.

Health care providers should actively engage pa-tients in formulating a care plan104 that includes theexpected frequency of follow-up visits with all pro-viders, including a clear designation of the role eachprovider will play (eg, screening for specific cancers,screening for other cancers, other preventative mea-sures, and ongoing comorbidity management). A for-mal care plan can be an important tool to facilitatecommunication and to outline required surveil-lance.105

Because cancer survivors have an increased risk oftreatment-related comorbid conditions, there is thepotential to involve virtually every medical specialtyin long-term cancer care. Ideally, specialists with aninterest in care of survivors and a basic understandingof chemotherapy and radiation side effects should beidentified. As noted, long-term management of can-cer survivors is hampered by the lack of surveillanceguidelines, including those that would be specialty-specific. Research that identifies long-term treat-ment-related effects could foster and contribute toguideline development and lead to improved overallcare for cancer survivors.

Organizing and Communicating HealthInformationTemplates for organizing treatment data and creatinga written survivor care plan at the end of treatmenthave been developed by a number of sources. Theseplans are based on a combination of the best availableclinical information, evidence-based standards, andin some cases, institutional practices. The IOM hassuggested a list of elements to be included in a careplan; however, lack of research makes it impossible todetermine, with any certainty, what should be in-cluded in a care plan. It has been noted that careplans are only as good as their contents, and there isconsiderable debate among the oncology care team asto who should be responsible for developing a per-sonalized plan for post-treatment care and whatshould be considered when developing that plan.

The development of a treatment summary and acare plan for survivors is challenging because it re-quires time and resources, 2 commodities that arehard to come by for busy oncology clinicians in the

current practice environment. One strategy would bethe adoption of electronic medical record (EMR)systems within institutions that would allow healthcare providers to communicate across specialties. Sys-tems that interface across institutions would signifi-cantly improve communication among medical pro-viders.

The EMR allows easy exchange of notes amongproviders and eliminates the need for every providerto document extensive medical information becausethis information is placed in the record at the initialencounter with a health care provider in the system,and needs only to be verified and updated at eachsubsequent encounter. The easy and efficient ex-change of information among providers allows pri-mary, specialty, and oncology care providers to sharethe management of these patients and will hopefullyimprove confidence among patients that they arereceiving optimal care.

Although it has been years since numerous groupscalled for the continuum of cancer care to includesurvivorship, it is evident that the adult oncologycommunity has been slow to embrace the concept.However, in recent years, several things have con-tributed to catapulting this phase of cancer care to thelevel of a medical specialty. The implementation ofthe EMR in many institutions has cleared a numberof barriers to providing seamless care to survivors byrevolutionizing communication among specialties,organizing patient data, educating patients and pro-viders, and billing more efficiently for services pro-vided. Advocacy groups and patients are demandingthat cancer care include the survivorship phase, andmany medical issues encountered by cancer survivorsthat were once considered normal comorbidities as-sociated with aging are now considered possible lateeffects of cancer treatment, and these must be ad-dressed by oncology, specialty, and primary care pro-viders.

Ideally, treatment summaries and survivorship careplans should serve as conduits between active cancercare and survivorship care and also between survivorsand providers. In our current health care system, thequestion of responsibility for the care of cancer sur-vivors among health care providers remains unclear.Is the medical oncologist, the primary care provider,the gynecologist, the surgeon, the radiation oncolo-gist, or another provider responsible for ensuring thatcancer survivors receive comprehensive medical care




Am

erican Cancer S


cancersoc.orgD

ownloaded from


FIGURE 1. American Society of Clinical Oncology (ASCO) Care Plan Template. HCP indicates health care provider; PCP, primary care provider. *Reflects numberof users for whom data is available according to version implementation. Reprinted with permission. (c) 2008 American Society of Clinical Oncology. www.asco.org




Am

erican Cancer S


cancersoc.orgD

ownloaded from


FIGURE 1. (Continued)




Am

erican Cancer S


cancersoc.orgD

ownloaded from


that attends to both screening for recurrent and/orprogressive disease and the management of routinehealth care and screening? Unfortunately, more thanhalf of primary care providers rate the transition processfrom oncology to primary care as fair or poor,8 and upto one-third of cancer survivors are unsure of whoamong their physicians is in charge of their follow-upcare.106 Although intended to assist in the care of sur-vivors, treatment summaries and survivorship care plansalso empower survivors to guide their own care and toensure that they receive recommended screening.

In the current health care environment of shrink-ing resources, questions about the time and costsurrounding care plan development and implemen-tation are important. Care plans must be individual-ized and detailed in order to be comprehensive.However, most health care providers have little timeto devote to their creation, even when much of theinformation and language can be obtained from ex-isting sources. In a recent survey-based study, mostoncologists reported that a survivor care plan toolshould require no more than 20 minutes per patient.7

Furthermore, no method of reimbursement cur-rently exists for creation of survivorship care plans byindividual centers. The IOM addressed this concern,recommending that survivorship care plan creation“be reimbursed by third-party payers of healthcare,”2

but this concept has yet to be realized in practice.

Planning Care for Adult CancerSurvivorsIn response to the call and to assist with the chal-lenges of caring for adult cancer survivors, advocacygroups, professional organizations, and cancer cen-ters have developed treatment summaries and survi-vor care plan templates, forms, and tools.107 Thefollowing describes a few of these efforts.

ASCO offers survivor care plan templates specificallyfor survivors of breast and colorectal cancers and ageneral template that can be used for any cancer diag-nosis. These templates can be completed online andsaved as Word (Microsoft, Redmond, Washington)documents, which allow the user to integrate ASCOrecommendations into the document to guide the careof cancer survivors.104 In this way, the template can beadapted to the specific needs of an individual cancersurvivor. The ASCO templates are available on theASCO Web site at http://www.asco.org.

Journey Forward is a program designed for pro-viders and patients who have recently completed ac-tive cancer treatment. This program was createdthrough the collaborative efforts of the National Co-alition for Cancer Survivorship, the UCLA CancerSurvivorship Center, WellPoint, Inc, and Genen-tech, and the plan that is generated by this programgives clear steps for providing are to survivors. Itbegins with a simple, yet complete, treatment sum-mary and offers recommendations for monitoringfuture care. Journey Forward kits are available onlineat http://www.JourneyForward.org, and they are tai-lored to oncologists, patients, and primary care phy-sicians. Journey Forward focuses on survivors ofbreast and colon cancers and has plans to expand toother cancer diagnoses.

The Cancer Survivor’s Prescription for Living is atemplate developed by and for nurses in oncologicalpractices. This template, printed in the April issue ofthe American Journal of Nursing108 outlines cancertreatment history, significant problems related to orpresenting as late effects of treatment, and otherhealth issues. This survivor care plan includes guide-lines for addressing persistent physical and psychos-ocial issues. It is recommended that health promo-tion and disease prevention measures, includingrecommended cancer screening activities, be outlinedby the user on this template. However, this rathercomprehensive template (available at http://tiny.cc/SFA8e) requires handwritten input of treatment anddisease information and is not currently available inan electronic version that allows easy input and mod-ification or saving of information entered.

A number of institutions are developing and imple-menting their own internal treatment summary and/orconsensus-driven survivor care plan templates, includ-ing the Abramson Cancer Center at the University ofPennsylvania, Fred Hutchinson Cancer Research Cen-ter, Memorial Sloan-Kettering Cancer Center (http://tiny.cc/rqgxq), the University of Colorado Cancer Cen-ter, and the Dana Farber Cancer Institute. Thesedocuments can be obtained by contacting individualsconnected to the cancer survivor programs at each giveninstitute (personal communications).

With the tremendous growth of Internet-basedtechnology during the last decade, numerous cancerinformation Web sites and links to educational ma-terials developed by professional organizations havebeen made available to cancer survivors and provid-




Am

erican Cancer S


cancersoc.orgD

ownloaded from


ers. In May 2007, prior to the development of thetemplates described thus far, the first Internet-basedtool for creation of individualized survivor care planswas launched. This plan tool was initially namedOncoLife. Its developers recently partnered with theLance Armstrong Foundation to release a revisedversion as the LIVESTRONG Care Plan poweredby Penn Medicine’s OncoLink (http://www.lives-trongcareplan.org). This care plan was developed as apatient-oriented tool and has the potential to evolveinto a multiversion mechanism that will allow thegeneration of several versions of a care plan that willmore appropriately meet the differing needs of pa-tients and providers. As end-users are expected toinclude patients, it is important to note that the careplan is not intended to replace provider recommen-dations, and users are advised on the Web site todiscuss the information with their medical team.

The LIVESTRONG Care Plan can be completedby survivors, families, or providers, and a variety ofuser-specific questions are included and modified witheach new version based on survivor and clinician feed-back. After entry of demographic, disease, and treat-ment information, users receive a comprehensive, indi-vidualized list of recommendations specific to primarycancer diagnoses and treatments received. These rec-ommendations are evidence- or consensus-based,whenever possible, and are in concordance with guide-lines provided by the IOM, COG, NCI, and ASCO.In areas in which evidence- or consensus-based guide-

lines are not available, recommen-dations are based on practice atthe developer’s institution.

Questions regarding whetherpatients need to enter specificdoses of chemotherapy agents andradiation received have arisen. Be-cause, at this time, there is no ev-idence that knowledge of specificdoses influences the risk of lateeffects or that this knowledgewould lead to specific recommen-dations for screening,111,112 theOncoLink team that developed thetool decided that this informationwould not be required. Many in-stitutions and providers choose toinclude this treatment informa-

tion in the cancer treatment summaries that they develop.Before the launch of the care plan program, the OncoLinkteam obtained permission from the University of Penn-sylvania Institutional Review Board to collect data whilemaintaining user anonymity. The intent was forthese data to guide the evolution and revisions ofthe LIVESTRONG Care Plan. To date, there isnothing in the literature that describes users ofonline care plans. Consequently, we report thesedescriptive data in figures 2, 3, and 4.

To date, almost 6000 users have completed the In-ternet care plan (Figure 1). Users identified themselvesas survivors, friends or family of survivors, and healthcare providers (primarily nurses or nurse practitioners).Most respondents were Caucasian, female, and well-educated. The most common cancer diagnosis wasbreast cancer, followed by hematologic and gastrointes-tinal malignancies (Figure 2). Data from Internet utili-zation studies have demonstrated this demographic rangeto be the most likely to use the Internet for health infor-mation, including information about cancer.111-114 MostLIVESTRONG Care Plan users reported some combi-nation of having undergone surgery, chemotherapy, andradiation. One-third of these survivors reported that theyreceive follow-up care from oncologists and primary careproviders, with approximately one-half receiving follow-upcare solely from oncologists. It is noteworthy that few usersreported receiving survivor information previously, beingcared for at a cancer center with a dedicated survivorprograms, or knowing whether such a program even ex-isted.

FIGURE 2. Demographics of LIVESTRONG Care Plan Users are listed.




Am

erican Cancer S


cancersoc.orgD

ownloaded from


Earle17 stated that it is crucial for the research com-munity to evaluate each element of the survivorship careplan. He also recommends observational studies to de-termine the knowledge and desire demonstrated bycancer survivors for information about the elements of aproposed care plan. Level of satisfaction with the infor-mation provided, the transition from the treatment tothe survivor phase of care, and other issues were in-cluded in Earle’s suggestions for research that should beconducted in conjunction with widespread develop-ment and implementation of survivorship care plans.

In July 2008, an optional user-satisfaction survey wasadded to the LIVESTRONGCare Plan. Based on informationfrom 747 users, care plan develop-ment required an average of 6.2minutes. Overall, cancer survivorsreported high satisfaction with thecare plan. Most reported that theyhad the information needed togenerate the care plan, that theinformation provided was helpful,and that they planned to share thecare plan with their health careprovider. Information overloaddid not appear to be a problemoverall, although a substantial mi-nority reported wanting some-what more information. Mosthealth care providers reported thatthey would use the program with

future patients (Figure 3). Thesedata can be a useful resource forinstitutions and groups who areworking to develop templates forsurvivors’ treatment summariesand care plans.

As institutions struggle to de-velop templates and/or to adaptand use existing ones, it is impor-tant to remember that there is noperfect approach to the develop-ment of treatment summaries orcare plans for cancer survivors. In-stitutions differ in their resources,and surveillance guidelines areonly beginning to become avail-able, creating reason for pausewhen putting resources into the

generation of formal care plans for cancer survivors.However, as Earle17 noted, “even informal plans can besufficient to improve the quality of care for a survivor.”

ConclusionOncology clinical practices focus on treatment andmanagement of malignant diseases, and follow-up visitsfor patients who have completed treatment are generallydirected toward surveillance for recurrent disease. Con-sequently, there is often inadequate assessment andmanagement of symptoms reported by survivors that

FIGURE 3. Cancer Diagnoses of LIVESTRONG Care Plan Users are shown.

FIGURE 4. LIVESTRONG Care Plan Queries are illustrated. *Query posed to survivor/friends/family members.†Query posed to health care providers only.




Am

erican Cancer S


cancersoc.orgD

ownloaded from


may be related to the cancer treatment they received. Inmany cases, symptoms and medical issues that arise inthis population are viewed as expected comorbidities ofaging and subsequently referred to ill-prepared provid-ers of primary and specialty care for management. Sur-vivors may hesitate to present issues to their oncologycare providers by thinking that they are nononcologyproblems and, to some extent, that their oncology pro-viders are not willing or equipped to deal with theseproblems.13 Many survivors also report concern thattheir providers are too busy with patients in treatmentto address a survivor’s seemingly less significant issues.

The provision of survivor care as a component ofcancer care, translational research that guides that care,and the education of patients, providers, and the publicare critical to the development of the adult cancer sur-vivor field. Numerous reports that examine the broadarray of survivor issues outline recommendations for thedevelopment of treatment summaries and care plans,and models of care, as well as the need to change theeducation of professionals caring for cancer survivors.These reports also address the need for translationalresearch that will inform and guide clinical care.

It seems that oncologists have been abruptlyconfronted with a population of patients whosedemands differ from those of patients under treat-ment and whose numbers are out of control. Formany years, the oncology community engaged inthe treatment of adults chose to ignore or dismissthe need for care to include patients who were nolonger being actively treated. Cancer survivor carerequires a thoughtful, organized approach to ad-dress recommendations made by the IOM andother groups. However, the current number ofsurvivors who require follow-up care poses signif-icant and immediate challenges to the medicalcommunity as this population grows. Resources are

limited and shrinking at a time when patients andproviders are demanding evidence-based guide-lines for surveillance and the necessary care ofcancer survivors. The IOM recognized that, de-spite the lack of data to support their use, careplans should be developed for every cancer survi-vor2; however, this is an added burden on thealready overextended decreasing population of pro-viders of oncology care. In addition, it is necessaryto develop survivorship care plans by using surveil-lance and follow-up recommendations based onconsensus and clinical evidence, but this will not bea feasible long-term solution.

The cancer survivor literature has exploded duringthe last few years, highlighting the broad scope ofquestions to be researched in this very young field.However, research opportunities for addressing some ofthe crucial questions that might have a direct bearing onthe conduct of clinical care are still limited. The medicalcommunity is expected to provide care to cancer survi-vors without adequate data to make accurate and ap-propriate recommendations for follow-up, and al-though data to support these recommendations as wellas studies to support the efficacy of providing survivorcare in different settings by different providers is sorelyneeded, it is increasingly evident that it will be decadesbefore the field of survivor research is mature enough toproduce a body of literature that will guide clinical careas well as future research.

In the interim, clinical care will drive the initiationof research that examines the plethora of cancersurvivor issues; however, in the long run, transla-tional research must and will drive the clinical care ofcancer survivors. A paradigm shift in cancer carerequires that the survivorship phase of care be recog-nized as an essential and distinct phase in the con-tinuum of cancer care.

References1. Travis LB, Yahalom J. Cancer survivor-

ship. Preface. Hematol Oncol Clin NorthAm. 2008;22:xi-xii.

2. Hewitt M, Greenfield S, Stovall E, eds.From Cancer Patient to Cancer Survivor:Lost in Transition. Washington, DC: Na-tional Academies Press; 2006.

3. Hoffman B, Stovall E. Survivorship per-spectives and advocacy. J Clin Oncol.2006;24:5154-5159.

4. Stein K, Smith T, Kim Y, et al. The AmericanCancer Society’s studies of cancer survivors:the largest, most diverse investigation oflong-term cancer survivors so far. CancerNurs. 2006;29(2 suppl):83-85.

5. Landier W, Bhatia S, Eshelman DA, et al.Development of risk-based guidelinesfor pediatric cancer survivors: the Chil-dren’s Oncology Group Long-Term Fol-low-Up Guidelines from the Children’sOncology Group Late Effects Committeeand Nursing Discipline. J Clin Oncol.2004;22:4979-4990.

6. Patlak M, Levit L. Ensuring quality cancercare through the oncology workforce.Institute of Medicine, National CancerPolicy Forum. Washington, DC:NationalAcademies Press; 2009.

7. Hewitt M, Bamundo A, Day R, Harvey C.Perspectives on post-treatment cancer care:qualitative research with survivors, nurses,and physicians. J Clin Oncol. 2007;25:2270-2273.

8. Nissen MJ, Beran MS, Lee MW, et al.Views of primary care providers on fol-low-up care of cancer patients. Fam Med.2007;39:477-482.




Am

erican Cancer S


cancersoc.orgD

ownloaded from


9. Earle CC, Burstein HJ, Winer EP, Weeks JC.Quality of non-breast cancer health mainte-nance among elderly breast cancer survi-vors. J Clin Oncol. 2003;21:1447-1451.

10. Mao JJ, Bowman MA, Stricker CT, et al.Delivery of survivorship care by primary carephysicians: the perspective of breast cancerpatients. JClinOncol.2009;27:933-938.

11. Starfield B, Fryer GE Jr. The primary carephysician workforce: ethical and policy impli-cations.AnnFamMed.2007;5:486-491.

12. Erikson C, Salsberg E, Forte G, BruinoogeBA, Goldstein M. Future supply and de-mand for oncologists: challenges to assur-ing access to oncology services. J OncolPractice. 2007;3:79-86.

13. Earle CC, Neville BA. Under use of neces-sary care among cancer survivors. Cancer.2004;101:1712-1719.

14. Salsberg E, Grover A. Physician workforceshortages: implications and issues foracademic health centers and policymak-ers. Acad Med. 2006;81:782-787.

15. Salsberg ES, Forte GJ. Trends in thephysician workforce, 1980-2000. HealthAff (Millwood). 2002;21:165-173.

16. Shulman LN, Jacobs LA, Greenfield S, et al.Cancer care and cancer survivorship care inthe United States: will we be able to care forthese patients in the future. American Soci-ety of Clinical Oncology Journal of Oncol-ogy Practice Web site. jop.ascopubs.org. JOncol Pract. 2009;5:119-123.

17. Earle CC. Failing to plan is planning to fail:improving the quality of care with survi-vorship care plans. J Clin Oncol. 2006;24:5112-5116.

18. Hewitt M, Weiner S, Simone JV, eds.Childhood Cancer Survivorship: ImprovingCare and Quality of Life. Washington, DC:National Academies Press; 2003.

19. American Academy of Pediatrics Sectionon Hematology/Oncology Children’s On-cology Group. Long-term follow-up carefor pediatric cancer survivors. Pediatrics.2009;123:906-915.

20. Armenian SH, Bhatia S, Meadows AT. Lateeffects of childhood cancer therapy. In:Philip A. Pizzo DGP, eds. Principles andPractice of Pediatric Oncology. Vol 6.Philadelphia: Lippincott, Raven; 2009.

21. Meadows AT, D’Angio GJ, Evans AE, et al.Oncogenesis and other late effects ofcancer treatment in children. Radiology.1975;114:175-180.

22. Meadows A, Baum E, Fossati-Bellani F, et al.Second malignant neoplasms in children:an update from the Late Effects StudyGroup. J Clin Oncol. 1985;3:532-538.

23. Packer RJ, Meadows AT, Rorke LB, Gold-wein JL, D’Angio G. Long-term sequelaeof cancer treatment on the central nervoussystem in childhood. Med Pediatr Oncol.1987;15:241-253.

24. Green DM, Brecher ML, Lindsay AN, et al.Gonadal function in pediatric patientsfollowing treatment for Hodgkin’s dis-ease. Med Pediatr Oncol. 1981;9:235-244.

25. Meadows AT, Gordon J, Massari DJ, et al.Declines in IQ scores and cognitive dys-functions in children with acute lympho-blastic leukemia treated with cranial irra-dition. Lancet. 1981;2:1015-1018.

26. Kingston JE, Hawkins MM, Draper GJ, etal. Patterns of multiple primary tumoursin patients treated for cancer during child-hood. Br J Cancer. 1987;6:331-338.

27. Heyn R, Haeberlen V, Newton W, et al.Second malignant neoplasms in childrentreated for rhabdomyosarcoma. Inter-group Rhabdomyosarcoma Study Commit-tee. J Clin Oncol. 1993;11:262-270.

28. Breslow N, Takashima J, Whitton J, et al.Second malignant neoplasms followingtreatment for Wilm’s tumor: a report fromthe National Wilms’ Tumor Study Group.J Clin Oncol. 1995;13:1851-1859.

29. Bhatia S, Robison LL, Oberlin O, et al.Breast cancer and other second neoplasmsafter childhood Hodgkin’s disease. N EnglJ Med. 1996;334:745-751.

30. Link MP, Shuster JJ, Donaldson SS, BerardCW, Murphy SB. Treatment of childrenand young adults with early-stage non-Hodgkin’s lymphoma. N Engl J Med.1997;337:1259-1266.

31. Silber J, Radcliffe J, Peckham V, et al.Whole-brain irradiation and decline in intel-ligence: the influence of dose and age on IQscore. J Clin Oncol. 1992;10:1390-1396.

32. Hobbie WL, Stuber M, Meeske K, et al.Symptoms of posttraumatic stress in youngadult survivors of childhood cancer. J ClinOncol. 2000;18:4060-4066.

33. D’Angio DJ, Breslow N, Beckman B, et al.Treatment of Wilms’ tumor: results of theThird National Wilms’ Tumor Study. Can-cer. 1989;64:349-360.

34. Schellong G, Potter R, Bramswig J, et al.High cure rates and reduced long-termtoxicity in pediatric Hodgkin’s disease: TheGerman-AustrianMulticenterTrialDAL-HD-90. J Clin Oncol. 1999;17:3736-3744.

35. Loning L, Zimmermann M, Reiter A, et al.Secondary neoplasms subsequent to Ber-lin-Frankfurt-Munster therapy of acutelymphoblastic leukemia in childhood: sig-nificantly lower risk without cranial radio-therapy. Blood. 2000;95:2770-2775.

36. Oyharcabal-Bourden V, Kalifa C, GentetJC, et al. Standard-risk medulloblastomatreated by adjuvant chemotherapy fol-lowed by reduced-dose craniospinal radia-tion therapy: A French Society of PediatricOncology study. J Clin Oncol. 2005;23:4726-4734.

37. Packer RJ, Goldwein J, Nicholson HS, etal. Treatment of children with medullo-blastomas with reduced-dose craniospinalradiation therapy and adjuvant chemo-therapy: A Children’s Cancer Group study.J Clin Oncol. 1999;17:2127-2136.

38. Spreafico F, Bellani FF. Wilms tumor:past, present and (possibly) future. ExpertRev Anticancer Ther. 2006;6:249-258.

39. Corn B, Goldwein J, Evans I, D’Angio G.Outcomes in low-risk babies treated withhalf-dose chemotherapy according to theThird National Wilms’ Tumor Study. J ClinOncol. 1992;10:1305-1309.

40. Shusterman S, Meadows AT. Long termsurvivors of childhood leukemia. CurrOpin Hematol. 2000;7:217-222.

41. Robison LL, Armstrong GT, Boice JD, et al.The Childhood Cancer Survivor Study: aNational Cancer Institute-supported re-source for outcome and intervention re-search. J Clin Oncol. 2009;27:2308-2318.

42. Ganz PA. Pediatric cancer survivorship: theChildhood Cancer Survivor Study—editor’sforeword. J Clin Oncol. 2009;27:2307.

43. Robison LL, Mertens AC, Boice JD, et al.Study design and cohort characteristics ofthe Childhood Cancer Survivor Study: amulti-institutional collaborative project.Med Pediatr Oncol. 2002;38:229-239.

44. Armstrong GT, Liu Q, Yasui Y, et al. Latemortality among 5-year survivors of child-hood cancer: a summary from the Child-hood Cancer Survivor Study. J Clin Oncol.2009;27:2328-2338.

45. Leisenring WM, Mertens AC, ArmstrongGT, et al. Pediatric cancer survivorshipresearch: experience of the ChildhoodCancer Survivor Study. J Clin Oncol. 2009;27:2319-2327.

46. Cox CL, Hudson MM, Mertens A, et al.Medical screening participation in theChildhood Cancer Survivor Study. ArchIntern Med. 2009;169:454-462.

47. Oeffinger KC, Mertens AC, Sklar CA, et al.Chronic health conditions in adult survi-vors of childhood cancer. N Engl J Med.2006;355:1572-1582.

48. Ginsberg JP, Hobbie WL, Carlson CA,Meadows AT. Delivering long-term fol-low-up care to pediatric cancer survivors:transitional care issues. Pediatr BloodCancer. 2006;46:169-171.

49. Meadows AT. Pediatric cancer survivor-ship: research and clinical care. J ClinOncol. 2006;24:5160-5165.

50. Oeffinger KC, Wallace WH. Barriers tofollow-up care of survivors in the UnitedStates and the United Kingdom. PediatrBlood Cancer. 2006;46:135-142.

51. Oeffinger KC, McCabe MS. Models fordelivering survivorship care. J Clin Oncol.2006;24:5117-5124.

52. Kadan-Lottick NS, Robison LL, Gurney JG,et al. Childhood cancer survivors’ knowl-edge about their past diagnosis and treat-ment: Childhood Cancer Survivor Study.JAMA. 2002;287:1832-1839.

53. Bhatia S, Meadows AT. Long-term fol-low-up of childhood cancer survivors:futuredirection for clinical care and research.Pediatr Blood Cancer. 2006;46:143-148.

54. Mulrooney DA, Neglia JP, Hudson MM.Caring for adult survivors of childhoodcancer. Curr Treat Options Oncol. 2008;9:51-66.56.

55. Freyer DR, Brugieres L. Adolescent andyoung adult oncology: transition of care.Pediatric Blood & Cancer. 2008;50(S5):1116-1119.

56. Werba BE, Hobbie W, Kazak AE, et al.Classifying the intensity of pediatric can-cer treatment protocols: the intensity oftreatment rating scale 2.0 (ITR-2). PediatrBlood Cancer. 2007;48:673-677.

57. Rowland JH. Cancer survivorship: rethink-ing the cancer control continuum. SeminOncol Nurs. 2008;24:145-152.

58. Yabroff KR, Lawrence WF, Clauser S,Davis WW, Brown ML. Burden of illnessin cancer survivors: findings from a popu-lation-based national sample. J Natl Can-cer Inst. 2004;96:1322-1330.

59. Demark-Wahnefried W, Pinto BM, GritzER. Promoting health and physical func-tion among cancer survivors: potential forprevention and questions that remain.J Clin Oncol. 2006;24:5125-5131.

60. Ganz PA. Monitoring the physical healthof cancer survivors: a survivorship-fo-cused medical history. J Clin Oncol. 2006;24:5105-5111.

61. Carver JR, Ng A, Meadows AT, VaughnDJ. Cardiovascular late effects and theongoing care of adult cancer survivors. DisManag. 2008;11:1-6.

62. Schatzkin A. Can biomarkers help usunderstand the nutritional and lifestyle




Am

erican Cancer S


cancersoc.orgD

ownloaded from


factors important in cancer prognosis? JNutr. 2007;137(1 suppl):249S–252S.

63. Travis LB, Rabkin CS, Brown LM, et al.Cancer survivorship—genetic susceptibil-ity and second primary cancers: researchstrategies and recommendations. J NatlCancer Inst. 2006;98:15-25.

64. Institute of Medicine (IOM). Adler N, PageA, ed. Cancer Care for the Whole Patient:Meeting Psychosocial Health Needs. Wash-ington, DC: National Academies Press;2008.

65. Avis NE, Deimling GT. Cancer survivor-ship and aging. Cancer. 2008;113 (12suppl):3519-3529.

66. Nathan PC, Ford JS, Henderson TO, et al.Health behaviors, medical care, and inter-ventions to promote healthy living in theChildhood Cancer Survivor Study cohort.J Clin Oncol. 2009;27:2363-2373.

67. Eakin EG, Youlden DR, Baade PD, et al.Health status of long-term cancer survi-vors: results from an Australian popula-tion-based sample. Cancer Epidemiol Bi-omarkers Prev. 2006;15:1969-1976.

68. Clarke SA, Eiser C. Health behaviours inchildhood cancer survivors: a systematicreview. Eur J Cancer. 2007;43:1373-1384.

69. Florin TA, Fryer GE, Miyoshi T, et al.Physical inactivity in adult survivors ofchildhood acute lymphoblastic leukemia:a report from the childhood cancer survi-vor study. Cancer Epidemiol BiomarkersPrev. 2007;16:1356-1363.

70. Demark-Wahnefried W, Werner C, Clipp EC,et al. Survivors of childhood cancer and theirguardians.Cancer.2005;103:2171-2180.

71. Eaton D, Kann L, Kinchen S, et al. Youth riskbehavior surveillance—United States, 2007.MMWR Surveill Summ. 2008;57:1-131.

72. NicklasTA,O’NeilCE,FulgoniVLIII.Theroleof dairy in meeting the recommendations forshortfall nutrients in the American diet. J AmCollNutr.2009;28(suppl1):73S–81S.

73. Yeazel MW, Oeffinger KC, Gurney JG, etal. The cancer screening practices of adultsurvivors of childhood cancer: a reportfrom the Childhood Cancer Survivor Study.Cancer. 2004;100:631-640.

74. Oeffinger KC, Ford JS, Moskowitz CS, etal. Breast cancer surveillance practicesamong women previously treated withchest radiation for a childhood cancer.JAMA. 2009;301:404-414.

75. Emmons K, Li FP, Whitton J, et al.Predictors of smoking initiation and cessa-tion among childhood cancer survivors: areport from the childhood cancer survivorstudy. J Clin Oncol. 2002;20:1608-1616.

76. Rourke MT, Hobbie WL, Schwartz L,Kazak AE. Posttraumatic stress disorder(PTSD) in young adult survivors of child-hood cancer. Pediatr Blood Cancer. 2007;49:177-182.

77. Finnegan L, Wilkie DJ, Wilbur J, et al.Correlates of physical activity in youngadult survivors of childhood cancers. On-col Nurs Forum. 2007;34:E60–E69.

78. Lee YL, Santacroce SJ, Sadler L. Predictorsof healthy behaviour in long-term survi-vors of childhood cancer. J Clin Nurs.2007;16:285-295.

79. Lown EA, Goldsby R, Mertens AC, et al.Alcohol consumption patterns and risk fac-tors amongchildhoodcancer survivors com-

pared to siblings and general populationpeers. Addiction. 2008;103:1139-1148.

80. Blanchard CM, Courneya KS, Stein K.American Cancer Society’s SCS-II. Cancersurvivors’ adherence to lifestyle behaviorrecommendations and associations withhealth-related quality of life: results fromthe American Cancer Society’s SCS-II.J Clin Oncol. 2008;26:2198-2204.

81. Bellizzi KM, Rowland JH, Jeffery DD,McNeel T. Health behaviors of cancersurvivors: examining opportunities forcancer control intervention. J Clin Oncol.2005;23:8884-8893.

82. Findley P, Sambamoorthi U. Preventivehealth services and lifestyle practices incancer survivors: a population health in-vestigation. J Cancer Surviv. 2009;3:43-58.

83. Coups EJ, Ostroff JS. A population-basedestimate of the prevalence of behavioralrisk factors among adult cancer survivorsand noncancer controls. Prev Med. 2005;40:702-711.

84. Mayer D, Terrin N, Menon U, et al.Screening practices in cancer survivors. JCancer Surviv. 2007;1:17-26.

85. Trask PC, Rabin C, Rogers ML, et al. Cancerscreening practices among cancer survi-vors. Am J Prev Med. 2005;28:351-356.

86. NCI. Assessing progress, advancing change.President’s cancer panel 2005-2006 an-nual report. Bethesda, MD: Department ofHealth and Human Services, NationalInstitutes of Health; 2006.

87. Murthy VH, Krumholz HM, Gross CP.Participation in Cancer Clinical Trials:Race-, Sex-, and Age-Based Disparities.JAMA. 2004;291:2720-2726.

88. Warren JL, Mariotto AB, Meekins A,Topor M, Brown ML. Current and futureutilization of services from medical oncolo-gists. J Clin Oncol. 2008;26:3242-3247.

89. Kindig DA. Strategic issues for managingthe future physician workforce. BaxterHealth Policy Rev. 1996;2:149-182.

90. Goodman DC, Fisher ES. Physician workforcecrisis?Wrong diagnosis, wrong prescription.N Engl J Med. 2008;358:1658-1661.

91. Snyder CF, Earle CC, Herbert RJ, et al.Trends in follow-up and preventive carefor colorectal cancer survivors. J GenIntern Med. 2008;23:254-259.

92. Keating NL, Landrum MB, Guadagnoli E,Winer EP, Ayanian JZ. Surveillance test-ing among survivors of early-stage breastcancer. J Clin Oncol. 2007;25:1074-1081.

93. Carver JR, Shapiro CL, Ng A, et al.American Society of Clinical Oncologyclinical evidence review on the ongoingcare of adult cancer survivors: cardiac andpulmonary late effects. J Clin Oncol. 2007;25:3991-4008.

94. Mao JJ, Armstrong K, Bowman MA, et al.Symptom burden among cancer survi-vors: impact of age and comorbidity. J AmBoard Fam Med. 2007;20:434-443.

95. Grunfeld E. Primary care physicians andoncologists are players on the same team.J Clin Oncol. 2008;26:2246-2247.

96. Del Giudice ME, Grunfeld E, Harvey BJ,Piliotis E, Verma S. Primary care physicians’views of routine follow-up care of cancersurvivors. J Clin Oncol. 2009;27:3338-3345.

97. Cheung WY, Neville BA, Cameron DB,Cook EF, Earle CC. Comparisons of patient

and physician expectations for cancersurvivorship care. J Clin Oncol. 2009;27:2489-2495.

98. Grunfeld E, Urquhart R, Mykhalovskiy E, etal. Toward population-based indicators ofquality end-of-life care: testing stakeholderagreement. Cancer. 2008;112:2301-2308.

99. Grunfeld E, Levine MN, Julian JA, et al.Randomized trial of long-term follow-upfor early-stage breast cancer: a compari-son of family physician versus specialistcare. J Clin Oncol. 2006;24:848-855.

100. Horning SJ. Follow-up of adult cancersurvivors: new paradigms for survivor-ship care planning. Hematol Oncol ClinNorth Am. 2008;22:201-210, v.

101. Snyder CF, Frick KD, Kantsiper ME, et al.Prevention, screening, and surveillancecare for breast cancer survivors comparedwith controls: changes from 1998 to 2002.J Clin Oncol. 2009;27:1054-1061.

102. Grunfeld E. Looking beyond survival: howare we looking at survivorship? J ClinOncol. 2006;24:5166-5169.

103. Wattchow DA, Weller DP, Esterman A, etal. General practice vs surgical-based fol-low-up for patients with colon cancer:randomised controlled trial. Br J Cancer.2006;94:1116-1121.

104. Ganz PA, Casillas J, Hahn EE. Ensuringquality care for cancer survivors: imple-menting the survivorship care plan. SeminOncol Nurs. 2008;24:208-217.

105. Nekhlyudov L. “Doc, Should I See You orMy Oncologist?” a primary care perspectiveon opportunities and challenges in provid-ing comprehensive care for cancer survi-vors. J Clin Oncol. 2009;27:2424-2426.

106. Miedema B, MacDonald I, Tatemichi S.Cancer follow-up care. Patients’ perspec-tives. Can Fam Physician. 2003;49:890-895.

107. Houlihan NG. Transitioning to cancer survi-vorship: plans of care. Oncology Nurse Edi-tion. 2009;23:42-48. Cancer Network.comWebsite. http://www.cancernetwork.com/display/article/10165/1434523?verify�0.

108. Haylock PJ, Mitchell SA, Cox T, Temple SV,Curtiss CP. The cancer survivor’s prescrip-tion for living. Am J Nurs. 2007;107:58-70.

109. Cox CL, Rai SN, Rosenthal D, Phipps S,Hudson MM. Subclinical late cardiac toxic-ity in childhood cancer survivors: impacton self-reported health. Cancer. 2008;112:1835-1844.

110. Creutzig U, Diekamp S, Zimmermann M,Reinhardt D. Longitudinal evaluation ofearly and late anthracycline cardiotoxicityin children with AML. Pediatr Blood Can-cer. 2007;48:651-662.

111. Metz JM, Devine P, DeNittis A, et al. Amulti-institutional study of Internet utiliza-tion by radiation oncology patients. Int JRadiat Oncol Biol Phys. 2003;56:1201-1205.

112. Wilson JJ, Mick R, Wei SJ, et al. Clinicaltrial resources on the internet must bedesigned to reach underrepresented mi-norities. Cancer J. 2006;12:475-481.

113. van de Poll-Franse LV, van Eenbergen MC.Internet use by cancer survivors: currentuse and future wishes. Support Care Can-cer. 2008;16:1189-1195.

114. Fogel J, Ribisl KM, Morgan PD, Hum-phreys K, Lyons EJ. Underrepresentationof African Americans in online cancersupport groups. J Natl Med Assoc. 2008;100:705-712.




Am

erican Cancer S


cancersoc.orgD

ownloaded from


adult cancer survivorship: evolution, research, and planning ......childhood cancer survivors have...

Documents