AnakDevelopment of Risk-Based Guidelines For Pediatric

VOLUME 22 NUMBER 24 DECEMBER 15 2004
JOURNAL OF CLINICAL ONCOLOGY
From the Division of Pediatrics, City of

Hope Comprehensive Cancer Center,
Duarte; Department of Pediatric
Hematology-Oncology, Stanford University
Medical Center, Stanford; Division of
Hematology-Oncology, Department of
Pediatrics, USC Keck School of Medicine
and Childrens Hospital Los Angeles, CA;
Center for Cancer and Blood Disorders,
Childrens Medical Center; Department of
Family Practice and Community Medicine,
University of Texas Southwestern Medical
School, Dallas, TX; Division of Pediatric
Oncology, AFLAC Cancer Center and
Blood Disorders Service, Childrens Healthcare of Atlanta, Atlanta, GA; Department of
Hematology-Oncology, St. Jude Childrens
Research Hospital, Memphis, TN; Childrens Oncology Group Patient Advocacy
Committee, Lincoln, NE; Department of
Pediatrics, University of Miami School of
Medicine, Miami, FL; Division of Pediatric
Hematology-Oncology, University of North
Carolina, Chapel Hill, NC; Department of
Radiation Oncology, University of Rochester Medical Center, Rochester; Department
of Pediatrics, Roswell Park Cancer Institute,
Buffalo; Department of Pediatrics/Endocrinology, Memorial Sloan Kettering Cancer
Center, New York, NY; Department of
Radiation Oncology, McGill University
Health Centre, Montral, Qubec, Canada;
Department of Pediatric HematologyOncology, Childrens Hospital and Regional
Medical Center, Seattle, WA; Division of
Oncology, Childrens Hospital of Philadelphia, Philadelphia, PA; and Department of
Pediatrics, University of Minnesota School
of Medicine, Minneapolis, MN.
Submitted November 7, 2003; accepted
September 23, 2004.
Supported by the Childrens Oncology
Group grant U10 CA098543 from the
National Cancer Institute. Dr Hudson is also
supported by the Cancer Center Support
(CORE) grant CA 21765 from the National
Cancer Institute and by the American Lebanese Syrian Associated Charities.
Authors disclosures of potential conflicts of interest are found at the end of
this article.
Address reprint requests to Melissa M.
Hudson, MD, St Jude Childrens
Research Hospital, 332 N Lauderdale,
Memphis, Tennessee 38105; e-mail:
melissa.hudson@stjude.org.
2004 by American Society of Clinical
Oncology
0732-183X/04/2224-4979/$20.00
DOI: 10.1200/JCO.2004.11.032
S P E C I A L
A R T I C L E
Development of Risk-Based Guidelines for Pediatric

Cancer Survivors: The Childrens Oncology Group
Long-Term Follow-Up Guidelines From the Childrens
Oncology Group Late Effects Committee and
Nursing Discipline
Wendy Landier, Smita Bhatia, Debra A. Eshelman, Katherine J. Forte, Teresa Sweeney, Allison L. Hester,
Joan Darling, F. Daniel Armstrong, Julie Blatt, Louis S. Constine, Carolyn R. Freeman,
Debra L. Friedman, Daniel M. Green, Neyssa Marina, Anna T. Meadows, Joseph P. Neglia,
Kevin C. Oeffinger, Leslie L. Robison, Kathleen S. Ruccione, Charles A. Sklar, and Melissa M. Hudson
A
The Childrens Oncology Group Long-Term Follow-Up Guidelines for Survivors of Childhood,
Adolescent, and Young Adult Cancers are risk-based, exposure-related clinical practice
guidelines intended to promote earlier detection of and intervention for complications that
may potentially arise as a result of treatment for pediatric malignancies. Developed through
the collaborative efforts of the Childrens Oncology Group Late Effects Committee, Nursing
Discipline, and Patient Advocacy Committee, these guidelines represent a statement of
consensus from a multidisciplinary panel of experts in the late effects of pediatric cancer
treatment. The guidelines are both evidence-based (utilizing established associations between therapeutic exposures and late effects to identify high-risk categories) and grounded
in the collective clinical experience of experts (matching the magnitude of risk with the
intensity of screening recommendations). They are intended for use beginning 2 or more years
following the completion of cancer therapy; however, they are not intended to provide guidance
for follow-up of the survivors primary disease. A complementary set of patient education
materials (Health Links) was developed to enhance follow-up care and broaden the application
of the guidelines. The information provided in these guidelines is important for health care
providers in the fields of pediatrics, oncology, internal medicine, family practice, and gynecology,
as well as subspecialists in many fields. Implementation of these guidelines is intended to
increase awareness of potential late effects and to standardize and enhance follow-up care
provided to survivors of pediatric cancer throughout the lifespan. The Guidelines, and related
Health Links, can be downloaded in their entirety at www.survivorshipguidelines.org.
J Clin Oncol 22:4979-4990. 2004 by American Society of Clinical Oncology
INTRODUCTION
For several decades, the survival rates for

many childhood cancers have been improving at a remarkable pace, such that the overall cure rate for pediatric malignancies is
now over 75%.1 Currently, there are an estimated 270,000 survivors of childhood cancer
in the United States. About one individual in
1,000 is a childhood cancer survivor, and
among young adults age 20 to 34 years, an

estimated one in 570 individuals is a childhood
cancer survivor.2 The development of curative
therapy for most pediatric malignancies has
produced a growing population of childhood
cancer survivors who are at increased risk for a
variety of health problems resulting from their
cancer or its treatment.1,3,4 In children, some
cancer-related complications do not become
apparent until many years following cancer
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Copyright 2004 American Society of Clinical Oncology. All rights reserved.
Landier et al
treatment. As the population of childhood cancer survivors

enters adulthood, complications resulting from their cancer
therapy may be exacerbated by organ dysfunction that can
emerge as these survivors grow older.
Late effects, or therapy-related sequelae, that persist
or arise after completion of cancer therapy are commonly experienced by childhood cancer survivors.5-8 A
significant proportion of childhood cancer survivors are
likely to experience at least one late effect, which can be
severe or life-threatening in 25%.5,8 Late effects encompass a myriad of detrimental conditions including organ
dysfunction, psychosocial complications, and subsequent malignancies that may adversely impact a survivors quality of life and predispose them to early
mortality.9-14 Since many treatment sequelae may not
become clinically apparent until the survivor attains maturity or is affected by the aging process, the ability of
healthcare providers to anticipate late treatment effects is
essential in order to provide timely interventions to prevent or ameliorate cancer-related sequelae and their adverse effects on quality of life.
In contrast to the multitude of publications describing
treatment-related sequelae in childhood cancer survivors,
relatively few provide specific recommendations for health
screening and risk-reduction counseling to guide healthcare
providers in monitoring this vulnerable population.12,15-20
Developing recommendations for health screening of childhood cancer survivors has been difficult because of the evolving cancer therapies and late effects risk profiles; the long
latency needed to evaluate many of the health outcomes; the
multiple factors influencing cancer-related health risks; and
the generally unknown effects of aging on many treatment sequelae. These factors have resulted in a lack of
consensus regarding screening and risk reduction methods that could be used to guide healthcare providers,
survivors, and third party payers.
The salient issues influencing healthcare for childhood cancer survivors have been summarized in a recent
report organized by the Institute of Medicine entitled
Childhood Cancer Survivorship: Improving Care and
Quality of Life.2 The authors of this report recognized
childhood cancer survivors as a vulnerable group with
special healthcare needs that were not being optimally
addressed in the present healthcare environment, and
therefore called for the development of evidence-based
clinical practice guidelines for survivorship care. In response to these concerns, a collaborative task force from
the Childrens Oncology Group developed the LongTerm Follow-Up Guidelines for Survivors of Childhood, Adolescent, and Young Adult Cancers (COG-LTFU Guidelines)
in order to standardize and enhance follow-up care for pediatric cancer survivors.
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PRACTICE GUIDELINES
Clinical practice guidelines are systematically developed

statements to assist practitioner and patient decisions about
appropriate healthcare for specific clinical circumstances.21 The process of guideline development is outcomedriven, with the goal of providing recommendations that
benefit patients.22 The American Society of Clinical Oncology has identified three important patient outcomes
(survival, toxicity, and quality of life) in oncology guideline development, and acknowledges that long-term toxicity is particularly significant in pediatric oncology.23
Our article describes the development of clinical practice
guidelines to direct long-term follow-up care for pediatric cancer survivors.
GUIDELINE DEVELOPMENT
Background
The merger of the legacy pediatric cooperative clinical
trials groups into the Childrens Oncology Group (COG) in
the year 2000 resulted in a unique opportunity for collaboration among multidisciplinary experts in the late effects of
childhood cancer treatment. Following the National Cancer
Policy Boards meeting on childhood cancer survivorship in
January 2002, the Institute of Medicine charged the COG
with development of comprehensive clinical practice guidelines for long-term follow-up care of childhood cancer survivors. The methodology of the COG-LTFU guideline
development is reported here according to the specifications of the Conference on Guideline Standardization.24
Overview
The COG-LTFU Guidelines are risk-based, exposurerelated clinical practice guidelines for screening and management of late effects resulting from therapeutic exposures used
during treatment for pediatric malignancies. The guidelines
are both evidence-based (utilizing established associations between therapeutic exposures and late effects to identify highrisk categories) and grounded in the collective clinical
experience of experts (matching the magnitude of the risk with
the intensity of the screening recommendations). The screening recommendations in these guidelines represent a statement of consensus from a panel of experts in the late effects of
pediatric cancer treatment. Since therapeutic interventions for
a specific pediatric malignancy may vary considerably based
on the patients age, presenting features, and treatment era, a
therapy-based design was chosen to permit modular formatting of the guidelines by therapeutic exposure. The guidelines
are therefore organized according to therapeutic agent, and
cross-referenced to other topics with related toxicities. Importantly, the recommended periodic screening underscores the
use of a thorough history and physical examination (H&P) as
Pediatric Cancer Survivor Follow-Up Guidelines
the primary assessment for cancer-related treatment effects. In

this regard, 90 (88%) of the screening recommendations outlined for the 102 therapeutic exposures in the COG-LTFU
Guidelines are composed of assessments derived primarily
from the H&P, with 50 (49%) relying solely on the H&P and 23
(23%) relying on the H&P plus a baseline diagnostic study (eg,
lab, imaging), whereas 29 (28%) include periodic laboratory,
diagnostic imaging, or other testing. Interventions exceeding
minimal screening are provided for consideration in individuals with positive screening tests. Medical citations supporting
the association of each late effect with a specific therapeutic
exposure are indexed by section number and listed in the
reference section. Patient education materials complementing
the guidelines have been organized into Health Links that
feature health protective counseling on 33 topics, enhancing
patient follow-up visits and broadening application of the
guidelines. The COG-LTFU Guidelines and related Health
Links are available on the Childrens Oncology Group Web site
(www.survivorshipguidelines.org).
Goal
Implementation of these guidelines is intended to increase quality of life and decrease complication-related
healthcare costs for pediatric cancer survivors by providing
standardized and enhanced follow-up care throughout the
life span that (1) promotes healthy lifestyles, (2) provides
for ongoing monitoring of health status, (3) facilitates early
identification of late effects, and (4) provides timely intervention for late effects.
Target Population/Focus
The COG-LTFU Guidelines are intended for use beginning 2 or more years following the completion of cancer
therapy, and provide a framework for ongoing late effects
monitoring in childhood cancer survivors. However, these
guidelines are not intended to provide guidance for
follow-up of the pediatric cancer survivors primary disease.
The recommendations for periodic screening evaluations
provided in these guidelines are appropriate for asymptomatic survivors of childhood, adolescent, or young adult cancers who present for routine exposure-related medical
follow-up. More extensive evaluations are presumed, as
clinically indicated, for survivors presenting with signs and
symptoms suggesting illness or organ dysfunction.
Intended Users
The COG-LTFU Guidelines were developed as a resource for clinicians who provide ongoing healthcare to
survivors of pediatric malignancies. The information
within these guidelines is important for clinicians (eg, physicians, nurse practitioners, physician assistants, nurses) in
the fields of pediatrics, oncology, internal medicine, family
practice, and gynecology, as well as subspecialists in many
fields (eg, endocrinology, cardiology, pulmonology). A basic knowledge of ongoing issues related to the long-term
follow-up needs of this patient population is assumed.

Healthcare professionals who do not regularly care for
survivors of pediatric malignancies are encouraged to
consult with a pediatric oncology long-term follow-up
center if any questions or concerns arise when reviewing
or using these guidelines.
Developer/Funding Source
These guidelines were developed as a collaborative
effort of the Nursing Discipline and the Late Effects
Committee of COG, a National Cancer Institutesupported cooperative clinical trials group. All COG members have complied with the COG conflict of interest
policy, which requires disclosure of any potential financial or other conflicting interests.
Evidence Collection
Pertinent information from the published medical literature over the past 20 years (as of September 2003) was
retrieved and reviewed during the development of these
guidelines. For each therapeutic exposure, a complete
search was performed via MEDLINE (National Library of
Medicine, Bethesda, MD). Keywords included childhood
cancer therapy, complications, and late effects combined with keywords for each therapeutic exposure. References from the bibliographies of selected articles were used
to broaden the search.
METHODS
The leadership of the COG Late Effects Committee and

Nursing Discipline appointed a seven-member task force,
with representation from the Late Effects Committee,
Nursing Discipline, and Patient Advocacy Committee. The
task force was convened to review and summarize the medical literature and develop a draft of clinical practice guidelines to direct long-term follow-up care for pediatric cancer
survivors. The task force followed a modified version of the
process for guideline development established by the National Comprehensive Cancer Network, integrating available literature with expert opinion using reiterative
feedback loops.22 The original draft went through several
iterations within the task force before initial review. Multidisciplinary experts in the field, including nurses, physicians (pediatric oncologists and other subspecialists),
patient advocates, behavioral specialists, and other healthcare professionals were then recruited by the task force to
provide an extensive, targeted review of the draft, including
focused review of selected guideline sections. Revisions
were made based on these recommendations. The revised
draft was then sent out to additional multidisciplinary
experts for further review. A total of 62 individuals participated in the review process. The guidelines subsequently underwent comprehensive review and scoring by a
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16-member panel of experts in the late effects of pediatric

malignancies, composed of multidisciplinary representatives from the COG Late Effects Committee. In a parallel
effort led by the Nursing Clinical Practice Subcommittee,
complementary patient education materials (Health
Links) were developed. Each Health Link underwent two
levels of review, first by the Nursing Clinical Practice Subcommittee to verify accuracy of content and recommendations, and then by members of the Late Effects Committee
(to provide expert medical review) and Patient Advocacy
Committee (to provide feedback regarding presentation of
content to the lay public). The guideline development process is depicted in Figure 1. The membership relationships
between the task force, panel of experts, and reviewers is
illustrated in Figure 2, and a complete membership listing
for all of these groups is included in the Appendix.
Grading Criteria
The guidelines were scored by the multidisciplinary panel
of experts using a modified version of the National Comprehensive Cancer Network Categories of Consensus system (Table 1). Each score reflects the expert panels assessment of the
strength of data from the literature linking a specific late effect
with a therapeutic exposure, coupled with an assessment of the
appropriateness of the screening recommendation based on
the expert panels collective clinical experience. High-level
evidence (category 1) was defined as evidence derived from
high-quality case control or cohort studies. Lower-level evidence (category 2A and 2B) was defined as evidence derived
from nonanalytic studies, case reports, case series, and clinical
experience. Rather than submitting recommendations representing major disagreements, items scored as category 3
were either deleted or revised by the panel of experts to provide
Fig 1. Guideline development process.

COG, Childrens Oncology Group. *Sevenmember task force included representatives from the COG Nursing Discipline,
Late Effects Committee, and Patient Advocacy Committee (W.L., D.E., K.F., T.S.,
A.H., M.M.H., J.D.).
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Fig 2. Membership relationships between task force, review panel,

and reviewers.
at least a category 2B score for all recommendations included in the guidelines.

Prerelease Review
The initial version of the guidelines (Version 1.0
Childrens Oncology Group Late Effects Screening Guidelines) was released to the COG membership in March 2003
for a 6-month trial period. This allowed for initial feedback
in the form of targeted qualitative communications, resulting in additional review and revision of the guidelines by the
Late Effects Committee before public release.
Revisions
The guidelines were released to the public (Version
1.1Childhood Cancer Survivor Long-Term Follow-Up
Guidelines) on the COG Web site in September 2003. Following this release, clarification regarding the applicability
of the guidelines to the adolescent and young adult populations of cancer survivors was requested. In response, additional minor modifications were made and the title of the
guidelines was changed. The current version (Version 1.2
Long-Term Follow-Up Guidelines for Survivors of Childhood, Adolescent, and Young Adult Cancers) was released
to the public on the COG Web site in March 2004.
Plan for Updates
Development of any clinical care guidelines is a dynamic
process, requiring continual review and revision in order to
keep the document current and clinically meaningful. Multidisciplinary task forces have therefore been organized within
the COG Late Effects Committee to monitor the literature and
recommend changes to these guidelines as new information
becomes available. A total of 20 task forces have been organized to focus on specific clinical topics (eg, cardiovascular,
neurocognitive, fertility/reproductive, etc). Responsibilities of
these task forces include presentation of an annual report to
the Late Effects Committee describing new literature, and
preparation of recommendations for guideline revisions, such
as addition of agents/therapeutic exposures, revision of risk
groups, revision of screening recommendations, development
and/or modification of patient education materials, and modification of the reference list. The guidelines will be updated
annually to reflect changes recommended by these task forces.
Clinicians are advised to check the COG Web site periodically
for the latest updates and revisions to the guidelines (www.
survivorshipguidelines.org).
Definitions
Key terms critical for correct application of the COG-LTFU
guidelines include late effects, pediatric malignancies, and
consensus. Lateeffectsaredefinedastherapy-relatedcomplications or adverse effects that persist or arise after completion of
treatmentforapediatricmalignancy.Pediatricmalignanciesare
defined as those malignancies commonly associated with the pediatric population that may arise during childhood, adolescence,
oryoungadulthood.Consensusisdefinedasgeneralagreement
among the panel of experts. The COG-LTFU Guidelines are
organized into nine major categories; key terms defining those
categories are described in Table 2.
RECOMMENDATIONS AND RATIONALE
Screening and follow-up recommendations are organized by

therapeutic exposure and included throughout the guidelines.
Pediatric cancer survivors represent a relatively small but
growing population at high risk for various therapy-related
complications. Although several well-conducted studies on
Table 1. Categories of Consensus Scoring for the COG-LTFU Guidelines

Category
1
2A
2B
3
Statement of Consensus
There is uniform consensus of the panel that: (1) there is high-level evidence linking the late effect with the therapeutic exposure and (2)
the screening recommendation is appropriate based on the collective clinical experience of panel members.
There is uniform consensus of the panel that (1) there is lower-level evidence linking the late effect with the therapeutic exposure and
(2) the screening recommendation is appropriate based on the collective clinical experience of panel members.
There is non-uniform consensus of the panel that (1) there is lower-level evidence linking the late effect with the therapeutic exposure
and (2) the screening recommendation is appropriate based on the collective clinical experience of panel members.
There is major disagreement that the recommendation is appropriate.
NOTE. Uniform consensus: Near-unanimous agreement of the panel with some possible neutral positions; non-uniform consensus: The majority of panel
members agree with the recommendation; however, there is recognition among panel members that, given the quality of evidence, clinicians may choose
to adopt different approaches; high-level evidence: Evidence derived from high quality case control or cohort studies; lower-level evidence: Evidence derived
from non-analytic studies, case reports, case series, and clinical experience.
Abbreviation: COG-LTFU, Childrens Oncology Group Long-Term Follow-Up.
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Table 2. Organization of the COG-LTFU Guidelines

Section
Therapeutic agent
Potential late effects
Risk factors
Highest risk
Periodic evaluations
Minimum recommended
frequency
Health protective counseling
Considerations for further

testing and intervention
References
Content
The therapeutic intervention for malignancy, including chemotherapy, biotherapy, radiation therapy, surgery,
transfusion, or hematopoietic cell transplant.
Treatment complications arising or persisting following completion of therapy for a pediatric malignancy.
Host factors (eg, age, sex, race, genetic predisposition), treatment factors (eg, cumulative dose of
therapeutic agent, mode of administration, combinations of agents), medical conditions (eg, premorbid or
comorbid conditions), and health behaviors (eg, diet, smoking, alcohol use) that may increase risk of
developing the complication.
Those conditions (host factors, treatment factors, medical conditions and/or health behaviors) associated
with the highest risk for developing the complication.
Recommended screening evaluations that may assist in detecting late effects, including health history,
clinical exams, laboratory evaluations, diagnostic imaging studies, psychosocial assessments, or other
indicated evaluations.
Recommended minimum interval of periodic evaluations based on risk factors and magnitude of risk as
supported by medical literature and/or the combined clinical experience of the panel of experts.
Suggested patient counseling regarding measures to prevent/reduce risk or promote early detection of the
potential treatment complications. Health Links are health education materials designed specifically to
accompany selected sections of the guidelines in order to provide targeted health information for
survivors of pediatric malignancies.
Recommendations for further diagnostic evaluations beyond minimum screening for individuals with
positive screening tests, recommendations for consultation and/or referral, and/or recommendations for
management of exacerbating or predisposing conditions.
Medical citations, corresponding to each numbered section of the guidelines, that provide evidence for the
association of the therapeutic intervention with the specific treatment complication and/or evaluation of
predisposing risk factors. In addition, some general review articles have been included in the reference
section for clinician convenience.
large populations of childhood cancer survivors have demonstrated associations between specific exposures and late
effects, the size of the survivor population and the rate of
occurrence of late effects does not (and will not in the
foreseeable future) allow for clinical studies that would
assess the impact of screening recommendations on the
morbidity and mortality associated with the late effect.
Therefore, scoring of each exposure reflects the expert panels assessment of the level of literature support linking the
therapeutic exposure with the late effect, coupled with an
assessment of the appropriateness of the recommended
screening modality in identifying the potential late effect
based on the panels collective clinical experience.
Potential Benefits and Harms
Potential benefits of implementing these guidelines
into clinical practice include earlier identification of and
intervention for late onset therapy-related complications in
this at-risk population, potentially reducing or ameliorating the impact of late complications on the health status of
survivors. In addition, ongoing healthcare that promotes
healthy lifestyle choices and provides ongoing monitoring
of health status is important for all cancer survivors.
Potential harms of guideline implementation include
increased patient anxiety related to enhanced awareness of
possible complications, as well as the potential for falsepositive screening evaluations, leading to unnecessary further work-up. In addition, costs of long-term follow-up
care may be prohibitive for some patients, particularly those
4984
lacking health insurance, or those with insurance that does

not cover the recommended screening evaluations.
Patient Preferences
The COG recognizes that specific patient care decisions
are the prerogative of the patient, family, and healthcare
provider. These guidelines are therefore not intended to
replace clinical judgment or to exclude other reasonable
alternative follow-up procedures.
Implementation Considerations
Initial concerns regarding implementation of the
COG-LTFU Guidelines include the practicality and efficiency of applying these broad guidelines in individual clinical situations. Studies to address guideline implementation
and refinement are a top priority of the COG Late Effects
Committee, and proposals to study feasibility of guideline
use in limited institutions are currently underway. Issues to
be addressed include description of anticipated barriers to
application of the recommendations in the guidelines and
development of review criteria for measuring changes in
care when the guidelines are implemented. Additional concerns surround the lack of current evidence establishing the
efficacy of screening for late complications in pediatric
cancer survivors. While most clinicians believe that ongoing surveillance for these late complications is important in order to allow for early detection and intervention
for complications that may arise, development of studies
addressing the efficacy of this approach is imperative in
order to determine which screening modalities are optimal for asymptomatic survivors.
Cancer Screening Recommendations
The recommendations for cancer screening included
in the COG-LTFU Guidelines were derived from cancer
screening evaluations supported by the American Cancer
Society for standard risk populations. Clinicians are also
encouraged to consult recommendations from other organizations, such as the US Preventive Services Task
Force (http://www.ahrq.gov/clinic/serfiles.htm).25,26 The organization of cancer screening recommendations is summarized in Table 3.
Certain high-risk populations of childhood cancer survivors merit heightened surveillance due to predisposing
host, behavioral, or therapeutic factors. An example of this
is the excess risk of breast cancer in female survivors of
pediatric malignancy treated with chest radiation; this risk
has been confirmed in numerous studies.9,27-34 Early initiation of breast cancer screening (beginning 8 years after
radiation or at age 25 years) was strongly supported by the
expert panel, despite the limitations associated with mammographic evaluation of the premenopausal breast. A similar concern was expressed about an excess risk of
gastrointestinal malignancies in survivors of pediatric malignancies treated with abdominal/pelvic radiation. Reports of
gastrointestinal malignancies in cohorts of long-term survivors suggest that radiation likely increases risk, but the median
age of onset is not as well established as that of secondary breast
cancer following chest radiation.28,35,36 The expert panel
agreed that early onset of screening likely was beneficial, but
decided a more prudent course would be to initiate screening
for colorectal cancer at age 35 years with modalities outlined by
the American Cancer Society.25
Sample Guideline and Evidence Base

The COG-LTFU Guidelines are organized to facilitate
identification of potential late effects associated with a specific therapeutic exposure. For example, a long-term survivor who received treatment with radiation involving the
thyroid gland is at risk for hypothyroidism from primary
gland failure (Fig 3).37-53 Thus, patients treated with totalbody irradiation, cervical, cranial, craniospinal, nasopharyngeal, oropharyngeal, mantle, mediastinal, whole lung,
and spinal fields should be evaluated for this complication.
The reported incidence of hypothyroidism in childhood
cancer survivors has varied widely depending on the primary diagnostic groups studied and the inclusion of cases of
subclinical hypothyroidism (elevated thyroid-stimulating
hormone with normal thyroxine).37-53 High cumulative
cervical radiation dose, particularly in excess of 20 Gy,
consistently increases the risk of hypothyroidism37-41,43-53;
however, reports evaluating the impact of other factors on
the risk of developing hypothyroidism after treatment for
pediatric cancer have been equivocal. While several adult
studies have observed an excess risk of hypothyroidism in
female compared to male survivors,37,38,40,43-46,49,51,53 this
relationship has been reported in only one cohort study of
pediatric cancer survivors.53 In addition to higher cumulative radiation dose and female sex, Childhood Cancer Survivors Study investigators identified age older than 15 years
at diagnosis and time greater than 5 years from diagnosis as
variables that independently affected the rate of hypothyroidism in a cohort of 1,791 survivors of pediatric
Hodgkins disease.53 Only one previous pediatric study observed a higher incidence of hypothyroidism in older adolescents, but this was confounded by the fact that older
patients were more likely to receive higher radiation doses.45 Finally, results regarding the effect of lymphography
Table 3. COG-LTFU Guidelines: Cancer Screening Recommendations

Section
Organ
At-risk population
Highest risk
Periodic evaluations
Content
The organ at risk for developing malignancy.
Populations generally considered at increased risk for the specified malignancy based on risk factors such as age, sex,
genetic susceptibility, personal or family history, health-related behaviors, or comorbidities.
Populations considered by the panel of experts or other evaluating bodies (such as the American Cancer Society) as
being at significantly increased risk for the specified malignancy. Risk factors may include therapeutic exposures
resulting from childhood cancer treatment, as well as other factors listed above (eg, genetic susceptibility).
Recommended screening evaluations including health history, clinical exams, laboratory evaluations, diagnostic
imaging studies, psychosocial assessments, or other indicated evaluations.
Standard risk: Guidelines provided under the standard risk category are per American Cancer Society
recommendations for standard-risk populations and are included for reference. In addition, clinicians are encouraged
to consult recommendations from other organizations, such as the US Preventive Services Task Force
(http://www.ahrq.gov/clinic/serfiles.htm).
Highest risk: Recommendations for these high-risk populations, when applicable, are specified and may differ from
recommendations for the standard risk groups due to the significantly increased risk of the specified malignancy
within the high-risk group.
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Fig 3. Sample excerpt from the Childrens Oncology Group Long-Term Follow-Up Guidelines for Survivors of Childhood, Adolescent, and Young Adult Cancers.
TSH, thyroid-stimulating hormone.
on long-term thyroid dysfunction are conflicting in both

pediatric and adult series.42,44,46,51
The time course for the development of hypothyroidism
has been similar across pediatric studies.37-40,44,45,48,50,51,53
Hypothyroidism most commonly presents during the first 5
years following radiation, but new cases have been reported as
late as 20 or more years following diagnosis of pediatric cancer.45 The higher incidence of subclinical thyroid dysfunction
observed in childhood cancer survivors compared with
healthy young adults underscores the need for screening of
asymptomatic patients.53
The COG-LTFU Guidelines outline the clinical manifestations of radiation-induced hypothyroidism and predisposing host and treatment factors (Fig 3). Clinical and
treatment factors associated with the highest risk of injury were identified through medical literature review of
currently available pediatric clinical investigations. The
recommended periodic evaluations represent routine
screening evaluations easily performed in a primary care
setting including a history, physical exam, and laboratory
evaluation with thyroid-stimulating hormone and free
thyroxine. Endocrine consultation for medical management of thyroid dysfunction is suggested as an additional
consideration for survivors presenting with abnormal
screening studies. A Health Link summarizing information about hypothyroidism and other thyroid disorders
manifesting after childhood cancer treatment is provided
to facilitate patient education. Finally, citations of seminal and review publications are outlined for clinicians
interested in more in-depth study of the literature.
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DISCUSSION
The development of curative therapy for most pediatric

malignancies has produced growing numbers of survivors
who are at increased risk for a variety of health problems
resulting from their cancer or its treatment. In order to
increase awareness of these potential health problems, and
in order to optimize and standardize care for this vulnerable
population, the COG has developed clinical practice guidelines for long-term follow-up of pediatric cancer survivors.
These guidelines are based on evidence linking therapeutic
exposures with specific late effects, as well as evidence of risk
factors (host-related, treatment-related, medical conditions, and health behaviors) that may increase the likelihood of developing those late effects. The identification of
patients at increased risk for late effects results is a compelling clinical need for the concurrent development of screening and management guidelines for those late effects, with
the onus on the guideline developer to provide those recommendations. Recognizing that there were no currently
available randomized clinical trials (and none forthcoming
in the foreseeable future) on which to base recommendations for periodic screening evaluations in this population,
the decision was made to draw on the collective clinical
experience of an expert panel in order to develop recommendations that matched the magnitude of risk with the
intensity of recommended screening. These clinical practice
guidelines therefore incorporate both evidence- and
consensus-based designs into a hybrid model (Fig 4), utilizing evidence from the literature to establish associations
Fig 4. Evidence-/consensus-based hybrid model for guideline development.
between therapeutic exposures and late effects, combined

with screening recommendations that match magnitude of
risk with intensity of screening and represent a statement of
consensus from a panel of experts in the late effects of
pediatric cancer treatment. Since optimal screening and
management for late effects in this population is not yet
defined, the recommendations are conservative and will be
modified as further evidence becomes available. It is anticipated that standardization of these guidelines will provide a
platform for determining the efficacy and cost-effectiveness
of screening in reducing morbidity and mortality from late
effects in this population, and a cadre of researchers within

the COG is committed to this effort. Ultimately, as with all
clinical guidelines, decisions regarding screening and clinical management for any specific patient should be individually tailored, taking into consideration the patients
treatment history, risk factors, comorbidities, and lifestyle.
The COG-LTFU Guidelines provide practical recommendations for evaluation and management of childhood cancer survivors who may be encountered across a
wide variety of healthcare settings. Integration of these
guidelines into clinical practice will promote increased
awareness of the unique healthcare needs of this specialized, growing, and maturing population of cancer survivors. This, in turn, should increase therapy-based
screening and evaluation for potential late effects with
subsequent early intervention when late effects are
detected. Implementation of these guidelines is intended
to standardize and enhance follow-up care provided
to survivors of pediatric malignancies throughout their
life span.

Authors Disclosures of Potential

Conflicts of Interest
The authors indicated no potential conflicts of interest.
Appendix
Childrens Oncology Group (COG) Long-Term Follow-Up Guidelines Task Force Members, Panel of Experts, Reviewers, and Health Link Authors
Affiliations
Task force members
Melissa M. Hudson, MD
Wendy Landier, RN, CPNP
Debra Eshelman, RN, CPNP
Kathy Forte, RN, CPNP
Joan Darling, PhD
Allison Hester, RN, CPNP
Teresa Sweeney, RN, CPNP
Panel of experts
Smita Bhatia MD, MPH
F. Daniel Armstrong, PhD
Julie Blatt, MD
Louis S. Constine, MD
Joan Darling, PhD
Carolyn R. Freeman, MB, BS, FRCPC
Debra L. Friedman, MD, MS
Daniel M. Green, MD
Wendy Landier, RN, CPNP
Neyssa Marina, MD
Anna T. Meadows, MD
Joseph P. Neglia, MD, MPH
Kevin Oeffinger, MD
Leslie L. Robison, PhD
Charles A. Sklar, MD
St Jude Childrens Research Hospital and the University of Tennessee College of Medicine, Memphis, TN
City of Hope Comprehensive Cancer Center, Duarte, CA
Childrens Medical Center, Dallas, TX
Childrens Healthcare of Atlanta, Atlanta, GA
Childrens Oncology Group Patient Advocacy Committee, Lincoln, NE
St Jude Childrens Research Hospital, Memphis, TN
St Jude Childrens Research Hospital and the University of Tennessee College of Medicine, Memphis, TN
University of Miami School of Medicine, Miami, FL
University of North Carolina, Chapel Hill, NC
University of Rochester Medical Center, Rochester, NY
Childrens Oncology Group Patient Advocacy Committee, Lincoln, NE
McGill University Health Centre, Montreal, Quebec, Canada
Childrens Hospital and Regional Medical Center, Seattle, WA
Roswell Park Cancer Institute, Buffalo, NY
Stanford University Medical Center, Stanford, CA
Childrens Hospital of Philadelphia, Philadelphia, PA
University of Minnesota School of Medicine, Minneapolis, MN
University of Texas Southwestern Medical School, Dallas, TX
University of Minnesota Cancer Center, Minneapolis, MN
Memorial Sloan Kettering Cancer Center, New York, NY
(continued on following page)
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Appendix
Childrens Oncology Group (COG) Long-Term Follow-Up Guidelines Task Force Members, Panel of Experts, Reviewers and Health Link Authors (continued)
Affiliations
Reviewers
Arlina Ahluwalia, MD
F. Daniel Armstrong, PhD
Lisa Bashore, RN, MS, CPNP
Smita Bhatia, MD, MPH
Julie Blatt, MD
Susan Bock, RN, BSN
Cathy Bourne, RN, BHSc(N)
Julianne Byrne, PhD
Hope Anne Castoria, RN, BSN
Laurie Cohen, MD
Louis S. Constine, MD
Lola Cremer, PT
Sarah Donaldson, MD
Patty Feist
Paul Fisher, MD
Carolyn R. Freeman, MB, BS, FRCPC
Daniel M. Green, MD
Mark Greenberg, MB, BCh
Wendy Hobbie, RN, MSN, CRNP
Nina Kadan-Lottick, MD, MSPH
Nancy Keene
Lisa B. Kenney, MD, MPH
Winnie Kittiko, RN, MS
Margaret Kulm, RN, MA
Missy Layfield
Marcia Leonard, RN, CPNP
Mary Leonard, MD, MSCE
Louis A. Leone, Esq
Neyssa Marina, MD
Leonard Mattano, MD
Anne Mauck, RN, MSN, CPNP
Charlene Maxen, RN, CNP
Lillian Meacham, MD
Anna T. Meadows, MD
Grace Powers Monaco, MD
Raymond Mulhern, PhD
John R. Mussman
Michael Neel, MD
Joseph P. Neglia, MD, MPH
Mary Nelson, RN, MS, CPNP
Kevin Oeffinger, MD
Roger Packer, MD
Arnold Paulino, MD
Rebecca D. Pentz, PhD
Leslie L. Robinson, PhD
David Rosenthal, MD
Kathy Ruble, RN, MSN, CPNP
Kathleen S. Ruccione, RN, MPH
Jean Sanders, MD
Cindy Schwartz, MD
Susan Shaw, RN, MS, PNP
Charles A. Sklar, MD
Jacquie Toia, RN, ND, CPNP
Deborah Waber, PhD
Susan L. Weiner, PhD
Fran Wiley, RN, MN
Suzanne L. Wolden, MD
Catherine L. Woodman, MD
Lise Yasui
Joseph Zins, PhD
Octavio Zavala
Northwestern University, Chicago, IL

University of Miami School of Medicine, Miami, FL
Cook Childrens Medical Center, Forth Worth, TX
Gundersen Lutheran Clinic, LaCrosse, WI
CancerCare Manitoba, Winnipeg, Manitoba, Canada
Childrens National Medical Center, Washington, DC
Hackensack University Medical Center, Hackensack, NJ
Dana Farber Cancer Institute, Boston, MA
University of Rochester Medical Center, Rochester, NY
Patient Advocate, Boulder, CO
McGill University Health Centre, Montreal, Quebec, Canada
Roswell Park Cancer Institute, Buffalo, NY
Hospital for Sick Children, Toronto, Ontario, Canada
Yale University School of Medicine, New Haven, CT
Patient Advocate, Annandale, VA
Dana-Farber Cancer Institute, Boston, MA
COG Patient Advocacy Committee, Douglasville, GA
COG Patient Advocacy Committee, Port Ludlow, WA
COG Patient Advocacy Committee, Cedar Falls, IA
C.S. Mott Childrens Hospital, Ann Arbor, MI
COG Patient Advocacy Committee, Walnut Creek, CA
Michigan State University, Kalamazoo, MI
Virginia Commonwealth University Health System, Richmond, VA
Childrens Hospital Medical Center - Akron, Akron, OH
Childhood Cancer Ombudsman Program, Heathsville, VA
COG Patient Advocacy Committee, Chicago, IL
University of Minnesota School of Medicine, Minneapolis, MN
Childrens Hospital Los Angeles, Los Angeles, CA
COG Patient Advocacy Committee, Atlanta, GA
University of Minnesota Cancer Center, Minneapolis, MN
Lucile Packard Childrens Hospital at Stanford, Palo Alto, CA
Johns Hopkins Hospital, Baltimore, MD
Childrens Hospital Los Angeles, Los Angeles, CA
State University of New York at Syracuse, Syracuse, NY
Childrens Memorial Medical Center, Chicago, IL
Boston Childrens Hospital, Boston, MA
The Childrens Cause, Inc., Silver Spring, MD
UCLA School of Medicine, Los Angeles, CA
University of Iowa Hospitals and Clinics, Iowa City, IA
COG Patient Advocacy Committee, Philadelphia, PA
COG Patient Advocacy Committee, Cincinnati, OH
COG Patient Advocacy Committee, Los Angeles, CA
(continued on following page)
4988
Appendix
Childrens Oncology Group (COG) Long-Term Follow-Up Guidelines Task Force Members, Panel of Experts, Reviewers and Health Link Authors (continued)
Affiliations
Health Link Authors
Julie Blatt, MD
Debra Eshelman, RN, MSN, CPNP
Sarah Friebert, MD
Sharon Frierdich, RN, MS, CPNP
Allison Hester, RN, MSN, CPNP
Nancy Keene
Asako Komiya, RN, MSN, PNP
Wendy Landier, RN, MSN, CPNP
Deborah Lafond, MS, RNCS, PNP
Marcia Leonard, RN, CPNP
Anne Mauck, RN, MSN, CPNP
Charlene Maxen, RN, CNP
Katherine Myint-Hpu, MSN, MPH, PNP
Kevin C. Oeffinger, MD
Kathy Ruble, RN, MSN, CPNP
Margery Schaffer, RN, MSN, CPNP
Susan Shannon, RN, MSN, CPNP
Teresa Sweeney, RN, MSN, CPNP
Sally Wiard, MSW, LCSW

Childrens Medical Center, Dallas, TX
University of Wisconsin Childrens Hospital, Madison, WI
Annandale, VA
C.S. Mott Childrens Hospital, Ann Arbor, MI
Virginia Commonwealth University Health System, Richmond, VA
Georgetown University Medical Center, Washington, DC
Childrens Medical Center, Dayton, OH
Miller Childrens Hospital, Long Beach, CA
Version 1.2 only.

Versions 1.0 and 1.1 only.
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VOLUME 22 NUMBER 24 DECEMBER 15 2004

JOURNAL OF CLINICAL ONCOLOGY

From the Division of Pediatrics, City of

Development of Risk-Based Guidelines for Pediatric

For several decades, the survival rates for

among young adults age 20 to 34 years, an

treatment. As the population of childhood cancer survivors

Clinical practice guidelines are systematically developed

Pediatric Cancer Survivor Follow-Up Guidelines

the primary assessment for cancer-related treatment effects. In

follow-up needs of this patient population is assumed.

The leadership of the COG Late Effects Committee and

16-member panel of experts in the late effects of pediatric

Fig 1. Guideline development process.

JOURNAL OF CLINICAL ONCOLOGY

Pediatric Cancer Survivor Follow-Up Guidelines

Fig 2. Membership relationships between task force, review panel,

at least a category 2B score for all recommendations included in the guidelines.

Screening and follow-up recommendations are organized by

Table 1. Categories of Consensus Scoring for the COG-LTFU Guidelines

Table 2. Organization of the COG-LTFU Guidelines

Considerations for further

Abbreviation: COG-LTFU, Childrens Oncology Group Long-Term Follow-Up.

lacking health insurance, or those with insurance that does

Pediatric Cancer Survivor Follow-Up Guidelines

Sample Guideline and Evidence Base

Table 3. COG-LTFU Guidelines: Cancer Screening Recommendations

Abbreviation: COG-LTFU, Childrens Oncology Group Long-Term Follow-Up.

on long-term thyroid dysfunction are conflicting in both

The development of curative therapy for most pediatric

Pediatric Cancer Survivor Follow-Up Guidelines

Fig 4. Evidence-/consensus-based hybrid model for guideline development.

between therapeutic exposures and late effects, combined

effects in this population, and a cadre of researchers within

Authors Disclosures of Potential

Northwestern University, Chicago, IL

JOURNAL OF CLINICAL ONCOLOGY

Pediatric Cancer Survivor Follow-Up Guidelines

University of North Carolina, Chapel Hill, NC

Version 1.2 only.

for Hodgkins disease. J Clin Oncol 16:35923600, 1998

20. Adams MJ, Hardenbergh PH, Constine

prospective cohort study. J Clin Oncol 20:

38. Chin D, Sklar C, Donahue B, et al: Thyroid

46. Kaplan MM, Garnick MB, Gelber R, et al:

JOURNAL OF CLINICAL ONCOLOGY

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