Survivors of childhood cancer are at increased risk for late effects of cancer therapy, but evidence suggests that adherence to follow-up care is suboptimal. Here, we review the barriers to adherence, including those unique to childhood cancer survivors, and the rationale for distribution of a survivorship care plan. We also discuss advantages and potential limitations of delivering survivorship care plans via web-based platforms, and describe the unique features of one of these platforms, Passport for Care. A baseline survey directed toward survivors and conducted through Passport for Care found that a significant proportion of survivors are unaware of their specific health risks resulting from cancer and its treatment, and compared with their parents, are less afraid of the risks of recurrence and of cancer therapy–associated late effects (n = 528). Web-based platforms such as Passport for Care have enormous potential for improving access to health information, as well as for enhancing patient, family caregiver, and healthcare provider awareness of both risks of late effects and recommended surveillance. Results from this survey also suggest the potential utility of leveraging these tools to conduct additional research on consenting survivors.
In the United States, survival of childhood and adolescent cancer has increased significantly over the past several decades, from fewer than 50% of patients in the 1970s to more than 80% currently. The number of childhood cancer survivors living in the United States has increased exponentially, and is projected to exceed 500,000 by 2020. However, the price of cure too often includes the burden of treatment-related morbidities. Seventy percent of adult survivors of childhood cancer are estimated to be affected by one or more severe, disabling, or life-threatening chronic medical conditions that significantly impact their quality of life.[3,4] The magnitude of risk for late effects of childhood cancer treatment is strongly tied to both host- and therapy-related factors. These primarily include the age of the child at the time of cancer diagnosis; the sex of the patient; a history of cancer-related surgery; exposure to, and dose of, specific chemotherapeutic agents; and/or field and dose of exposure to radiation.[5,6] The risk for these late effects increases substantially over the remaining lifetime of the survivor.[7,8] At 30 years after an initial cancer diagnosis, these late effects confer a twofold mortality risk compared with the general population. Given the potential lifelong impact of pediatric exposure to different anticancer agents and treatment modalities, survivors must be educated about the associated health risks and the benefit of forming an ongoing relationship with a medical provider, through routine visits to a primary care physician or to healthcare professionals at a cancer survivorship clinic.
Evidence-Based Guidelines for the Care of Childhood Cancer Survivors
In 2003, the Institute of Medicine (IOM) and the National Research Council National Cancer Policy Board issued a series of recommendations with the objective of improving the care of childhood cancer survivors and their quality of life; these recommendations included the development of evidence-based clinical practice guidelines. Subsequently, the first version of the Children’s Oncology Group Long-Term Follow-Up Guidelines for Survivors of Childhood, Adolescent, and Young Adult Cancers (COG LTFU Guidelines) was published in 2004, having been developed jointly by the COG Late Effects, Nursing Discipline, and Patient Advocacy committees. The COG LTFU Guidelines are freely available and targeted to healthcare professionals (http://www.survivorshipguidelines.org). They serve as a compendium of detailed, evidence-based information regarding the exposure-based risks for late effects after treatment of cancer in childhood or adolescence. Included with these guidelines are links to patient education materials (Health Links) and recommendations for routine surveillance. The COG LTFU Guidelines are updated approximately every 5 years, with the next update scheduled for release in 2018. There is an ongoing initiative, led by the International Late Effects of Childhood Cancer Guideline Harmonization Group, to synthesize these with other guidelines worldwide that have been developed for childhood cancer survivors.
Barriers to Follow-Up Care Adherence
Despite the inestimable value of the COG LTFU Guidelines, there are inherent challenges to their use and successful application in clinical practice. First, there are practical obstacles to sustaining into adulthood a complex medical record that details an illness diagnosed in childhood. Between 15% and 50% of adult survivors of childhood cancers have little to no recollection of specifics regarding their diagnosis, let alone the treatments they received as children.[13-16] Second, numerous physical and psychosocial barriers may contribute to poor survivor adherence to follow-up care—including, but not limited to, transportation and distance to the clinic, major life changes, lower socioeconomic status, lower educational level, lack of insurance coverage, work or school conflicts, and lack of time[17-21]—such that the number of survivors receiving cancer-related medical care continues to decline with increasing age.[22,23] As a result, survivors report suboptimal adherence to key surveillance recommendations within the COG LTFU Guidelines, such as regular mammograms for those exposed to chest irradiation, or general screening practices for those identified to be at highest risk for second malignant neoplasms.[24,25]
Consideration must also be given to survivor- and provider-related barriers when transitioning the medical care of an adolescent or young adult survivor of childhood cancer.[26,27] As pediatric cancer survivors age into adulthood, only about one-third continue to receive follow-up care at the institution where they were initially diagnosed, with the majority reporting transition to a primary care clinic.[22,28,29] With transition there is a substantial risk that key medical information affecting recommended surveillance and monitoring for late effects will be lost. Educational initiatives have been put in place to address these knowledge deficits among primary care providers, as well as a “shared care” model by which oncologists partner with generalists to improve adherence to follow-up recommendations.[31,32] Follow-up care that is administered in a cancer survivorship clinic has been associated with both improved adherence to the COG LTFU Guidelines and a reduced need for emergency medical care.[33,34] However, even among pediatric oncologists familiar with the COG LTFU Guidelines, one study found that only about one-third of specialist providers correctly answered questions regarding surveillance recommendations for the most common cancer therapy–related late effects, suggesting that even specialists may benefit from ongoing education and better access to the relevant guidelines.
Survivorship Care Plans (SCPs)
To address barriers to adherence and the gaps in knowledge among both specialists and primary care providers, in 2005 the IOM issued a recommendation that all cancer survivors receive an SCP. Elements considered integral to an acceptable SCP include a personalized treatment summary, information about possible long-term effects of cancer therapy and signs of recurrence, and general guidelines for follow-up care. Despite these recommendations, a significant number of childhood cancer survivors remain uninformed regarding their treatment history and risks for late effects. In a survey conducted in 2008 that included more than 8,000 participants from the National Cancer Institute–funded Childhood Cancer Survivor Study, only one-third had received medical care within the past 2 years that addressed late effects of their childhood cancer, and fewer than 20% reported receiving care that included elements of an acceptable SCP, such as risk reduction and screening. In 2011, approximately half of survivors recruited from the LIVESTRONG Survivorship Center of Excellence Network reported that they had not been given an SCP or even a treatment summary, despite the fact that 71% had received follow-up care through a survivorship clinic. Although the majority of COG institutions report providing survivors with detailed treatment summaries and surveillance recommendations, individual surveys of pediatric oncologists noted multiple barriers to delivering SCPs, such as insufficient time, resources, and support to generate the SCP, and a lack of expectation to do so. There is conflicting evidence as to whether receipt of a general written treatment summary, receiving medical care through a cancer survivorship clinic, or even directed educational interventions have a positive effect on the survivor’s working knowledge of his or her exposure history or risk for late effects.[39-43] However, when survivor education is simplified, tailored to personal risk, and limited to key late effects rather than presented as a general summary, survivors are able to demonstrate significant gains in both knowledge of their individual risks and adherence to risk-based screening.[44,45]
Failure of the oncologist to generate an SCP may negatively impact primary care provider adherence to evidence-based recommendations for follow-up care. While primary care physicians provide the bulk of long-term follow-up care to childhood cancer survivors, most report never receiving a treatment summary from either the patient or the treating oncologist.[46,47] Even those who do receive a treatment summary report discomfort with adhering to the recommendations outlined in SCPs due to lack of knowledge about and familiarity with information regarding specific cancers and their treatment, and/or insufficient training in delivery of this type of information to patients.[46-49] However, primary care providers are also more likely to report comfort with caring for childhood cancer survivors if they are provided with access to clinical care guidelines and surveillance recommendations. In fact, receipt of an SCP has been associated with a ninefold increased likelihood of scheduling an office visit that includes a discussion of survivorship care.
- Among childhood cancer survivors, survivorship care plan generation, delivery, and implementation remain suboptimal, which may impact adherence to long-term follow-up guidelines.
- Web-based platforms offer an opportunity to overcome barriers particularly evident among survivors of childhood cancer, such as a limited recollection of diagnosis and treatment or a transition of care that is complicated by the incomplete transfer of surveillance recommendations.
- Key objectives to consider when developing web-based platforms for survivorship care are that platforms be accurate and evidence-based; promote adherence by providing key, exposure-based recommendations; and be widely accessible and secure.
Delivery and implementation of SCPs remain suboptimal despite endorsement of SCP development by the IOM, survivor support for their use, positive feedback from clinicians, and several studies demonstrating the positive impact of a tailored SCP on adherence to recommendations outlined in the COG LTFU Guidelines.[51,52] These challenges echo known barriers to physician adherence to clinical practice guidelines, with general themes that include lack of awareness, lack of familiarity, lack of agreement, lack of self-efficacy, lack of outcome expectancy, and lack of an ability to overcome the inertia of previous practice. These general factors, compounded by specific factors such as the length and complexity of the COG LTFU Guidelines, act as barriers to the successful translation of these guidelines into clinical practice. There is a clear need for feasibility studies that assess potential roadblocks preventing the dissemination and adoption of evidence-based interventions, such as those represented by the COG LTFU Guidelines.
Delivery of SCPs Through Web-Based Systems
Society’s increasing reliance on the internet to facilitate obtaining health-related information, together with recent advances in healthcare technologies, have led to the development of numerous web-based systems designed to benefit cancer survivors. However, while a variety of SCP-generating internet-based tools are available for adult cancer survivors (eg, the OncoLife Survivorship Care Plan available through OncoLink [https://oncolife.oncolink.org] and the SCP builder and other resources offered by Journey Forward [https://www.journeyforward.org]), there are only a few publicized web-based systems designed specifically for survivors of childhood cancer. Notably, the limited published data available suggest that web-based systems improve survivor and provider satisfaction, understanding of health risks, and adherence to evidence-based guidelines for childhood cancer survivorship care.[55-57] These tools have been designed to support the medical provider, the survivor, and/or the caregiver, as will be described.
This survivor-centric web-based system (www.cancersurvivorlink.org) was developed at the Aflac Cancer and Blood Disorders Center in Atlanta, and supported through a grant from the Agency for Healthcare Research and Quality. The survivor or survivor’s caregiver is able to generate and maintain an electronic personal health record (ePHR) by uploading medical documents such as test results; alternately, an SCP can be generated by the survivor’s medical provider, by permitting a medical provider to upload documents on the survivor’s behalf.[56,58] Survivors may then access their medical record freely, retrieve documents, and access a virtual library of educational materials related to cancer survivorship. Survivors can also elect to share their ePHR with additional medical providers, as may be required for subspecialty care. This platform has been designed to promote survivor education of long-term health risks, and medical providers are also able to use this tool to access educational materials developed from the COG LTFU Guidelines, as well as survivor health records, with permission from the patient.
The Late Effects After Treatment Tool
This web-based, survivor-focused platform (http://leatt.thenccs.org) was developed through collaboration between clinicians at the National Children’s Cancer Society and St. Louis Children’s Hospital at Washington University School of Medicine. Similar to Cancer SurvivorLink, results can be saved in an individual user profile for future reference. Working from existing guidelines, as well as information provided by the user (eg, primary cancer diagnosis, age at diagnosis, sex, and treatment exposures), this tool generates succinct but comprehensive information about an individual’s risk for specific late effects. As an alternative to entering diagnosis and treatment information, survivors may report symptoms they are experiencing, to ascertain whether they may be related to late effects of cancer therapy. General recommendations are provided for follow-up care, as well as advice for risk reduction and directions and hours of operation of nearby childhood cancer survivor clinics. Similar to the Cancer SurvivorLink, the Late Effects After Treatment Tool may also be used by a parent/caregiver or medical professional, although it does not permit information stored in the survivor’s profile to be shared with other medical providers.
The Life After Childhood Cancer platform
Selected online platforms have been designed with the primary goal of improving the transition of care from the oncology clinic to general practitioners. One such example is Life After Childhood Cancer, a web-based system in the Netherlands that was developed for the University Medical Center Groningen. Using this platform, oncology providers generate the SCP based on the survivor’s medical record and guidelines from the Late Effects of Childhood Cancer task force of the Dutch Childhood Oncology Group (DCOG LATER study cohort). The SCP is then uploaded to the system, and both survivors who were treated at this institution and family doctors are provided with online access that is limited to the SCP.
The Passport for Care (PFC) system
In contrast to other platforms, the design of the PFC web-based system (https://www.passportforcare.org) is intended to support both survivors and healthcare professionals, by providing web-based access for both groups. PFC was initially developed as a clinical decision support tool by investigators from Baylor College of Medicine’s Center for Collaborative and Interactive Technologies and Texas Children’s Cancer and Hematology Centers, in collaboration with the COG Nursing Discipline and Late Effects committees, with funding that was provided by private donors, foundations, and the Cancer Prevention Research Institute of Texas. First released in 2007, PFC currently contains treatment summary information from more than 30,000 childhood cancer survivors. A total of 129 childhood cancer survivor clinics in the United States, as well as 6 clinics located outside of the United States, participate in PFC and enroll patients. PFC is closely linked with the COG LTFU Guidelines and, importantly, is updated with each new iteration of the guidelines, leveraging exposure-based algorithms to generate a detailed, comprehensive, and personally tailored SCP that is inclusive of current health risks, screening recommendations, and relevant educational materials (Figure 1). PFC also serves as a Health Insurance Portability and Accountability Act (HIPAA)-compliant database for storing personal health information. In 2015, a PFC Survivor website interface (https://cancersurvivor.passportforcare.org) was released in both English and Spanish; survivors are provided with access to their treatment history and a personally tailored SCP, as well as associated Health Links. On the PFC Survivor website, potential late effects and recommended follow-up testing are described in lay language and organized by body system. Efforts are underway to expand use of the PFC Survivor website and augment features that promote survivor/website interactivity.
Web-based platforms offer a unique opportunity to improve survivorship care by addressing many of the barriers to care experienced by survivors of childhood cancer, such as transition of care and lack of adherence to guidelines. Importantly, there is no cost associated with the use of any of the previously described platforms. Both Cancer SurvivorLink and the Late Effects After Treatment Tool are accessed directly through the website address. Life After Childhood Cancer is available free of charge to cancer survivors living in the Netherlands. The PFC Clinician website is available to any academic institution or private clinic treating survivors of childhood cancer worldwide. The PFC Survivor website is available to any survivor who wishes to participate; survivors may be enrolled by their treatment facility, medical provider, or by the PFC team, if they provide permission and relevant treatment records. Each of these web-based platforms offers the potential to foster survivor/medical provider and survivor/caregiver conversations regarding health risks related to cancer histories and treatment exposures, as well as emphasize the importance of adherence to the evidence-based COG LTFU Guidelines.
In developing these tools, a number of additional objectives warrant consideration:
• Ensure that demographic, diagnosis, and treatment exposure data are entered by, or at least verified by, the treating institution.
• Ensure that risk assessment and follow-up recommendations are based on current evidence-based and peer-reviewed guidelines.
• Produce a focused or comprehensive personalized SCP inclusive of a treatment summary, possible long-term effects of therapy, and follow-up recommendations.
• Provide relevant educational materials in lay language, available in multiple languages depending on the needs of the patient population.
• Promote survivor/caregiver and survivor/healthcare provider communication, and a forum for community discussion of issues relevant to cancer survivorship.
• Provide the tool such that cost is not a barrier to access (by making it either freely accessible or available at a low cost that is offset by the survivor’s medical insurance).
• Offer materials in both English and Spanish, with translation into other languages depending on the user population.
• Provide a secure environment for storage of personal health information.
• Ensure compatibility with both computers and smartphone devices.
Leveraging Web-Based Systems for Survivor Outreach
Web-based tools designed to support cancer survivors offer a valuable opportunity to identify and address survivors’ unmet needs. As an example of such an effort, we administered a survey through the PFC Survivor website that assessed knowledge of prior cancer history/treatments, knowledge of potential associated health risks, barriers to receiving follow-up care, and other domains. The survey was offered to either survivors or their parents/caregivers (if the survivor was younger than 18 years of age) at the time of initial login to the PFC Survivor website, and was restricted to Texas sites. Subjects were queried as to whether they would like to participate in research, and if they responded positively, were asked to complete a 26-question survey offered in Spanish or English. No incentive was offered for survey completion.
The survey results were as follows: among the 1,499 survivors or parents of survivors living in Texas who had logged in to the Survivor website (from 2015 through 2016), 886 consented to participate in research; of this group, 528 individuals completed the survey (for a response rate of 35.2%; Figure 2). Survey respondents included 213 survivors and 315 parents who were treated or whose children received treatment at 9 clinics in Texas. The self-reported demographic distribution was 86% White (with 49% self-identifying as Hispanic), 7% Black, 4% Asian, and 3% “other.” The majority of respondents were insured (93%), and 31% received their insurance through Medicaid. Twenty-seven percent reported household incomes below $25,000 per year, 18% had incomes between $25,000 and $50,000 per year, and the remainder reported incomes of more than $50,000 per year. Thirty percent of respondents had completed therapy for their primary cancer diagnosis more than 10 years prior to taking the survey, with the remainder having completed therapy within the past 10 years. As observed in prior studies, despite relatively high rates of adherence (with 92% of respondents reporting that they attended regular follow-up visits related to their cancer diagnosis), 69% of survivors and 40% of parents reported only moderate to no knowledge of the specific cancer therapy–related exposures. Moreover, 77% of survivors and 65% of parents reported only moderate to no knowledge regarding the potential late effects of cancer treatment. For survivors who reported poor adherence, the barriers identified echoed those found in previous studies, including busy schedule (40%), poor insurance coverage (23%), perception that follow-up is not needed (9%), and distance to clinic (14%).
With respect to parent and survivor attitudes and behaviors related to cancer, cancer therapy, and late effects, parents were significantly more likely than survivors to indicate fear of late effects (Mann-Whitney U test = 23,431; Z score = 4.971; P < .001) (Figure 3). Specifically, while 34% of parents reported feeling very afraid or extremely afraid of late effects or cancer recurrence, only 18% of survivors reported this same level of fear. Conversely, 60% of survivors reported feeling not at all afraid or only slightly afraid, compared with only 38% of parents. While previous studies have similarly reported ongoing psychological distress among parents of childhood cancer survivors, few have compared reported rates of fear between survivors and their parents. Given this observation, providers should acknowledge the need for ongoing psychological support for survivors and their parents, and be prepared to offer access to local available resources, such as support groups and consultation with a social worker or psychologist. The survey findings also suggest that survivors may have an inappropriately low level of concern about future health risk from their cancer treatment; their attitudes may reflect inadequate education or, conversely, a sense of invincibility from having survived a life-threatening disease.
A limitation to this study may be that survey participants were predominantly followed in an academic center or teaching hospital (> 90%), or in a cancer survivorship clinic. Therefore, participant demographics, reported knowledge of cancer and of risk for late effects, as well as perceptions or attitudes regarding individual risk may not reflect the larger population of childhood cancer survivors who are predominantly followed by primary care physicians in a nonacademic setting. This study did not assess the depth and extent of education provided to participant survivors and their families; however, there is a high likelihood that, compared with primary care clinics, academic cancer centers are better positioned to provide survivors with more detailed and extensive education about their disease and the short- and long-term effects of their specific courses of treatment. Nevertheless, survivors’ observed lack of knowledge about cancer and its associated late effects—and, similarly, their seeming lack of concern about their future health—may be even more prevalent in the wider cancer survivor population more likely to be followed by primary care providers.
The results of the PFC baseline survey suggest the existence of an unmet need for survivor and caregiver education that may be addressed through generation of an exposure-based SCP. However, more research is needed to test the impact of improved guideline adherence on specific healthcare outcomes, particularly those noted to be of greatest importance to survivors. For example, survivors may prefer an SCP that is targeted to specific risks with the largest potential health impact, rather than a comprehensive SCP inclusive of all potential risks, no matter how small. Our results also indicated that 59% of survivors who accessed the PFC agreed to participate in research, with a survey completion rate of 35%. This response rate suggests that it is feasible to conduct research through the PFC Survivor website, and that surveys may be utilized to evaluate survivors with diverse backgrounds, primary cancer diagnoses, and treatment exposure histories. Lastly, the survey has uncovered a significant unmet need for improved understanding of the perceptions and attitudes unique to young adult survivors of childhood cancer, and of how to best provide this specific population with survivorship support and education (for example, tools or techniques that improve communication between survivors and caregivers).
Potential Limitations of Web-Based Systems
Web-based platforms have enormous potential to access large populations of cancer survivors who may be receiving suboptimal follow-up care, due to either lack of education or lack of access to an informed medical provider. Moreover, these platforms offer the opportunity to leverage online tools that promote survivor education and healthy lifestyle behaviors beyond the information that is included in an SCP—including components such as e-learning, behavior-tracking, messaging, and social support. However, in a recent randomized controlled trial of childhood cancer survivors followed in a survivorship clinic, survivors who were randomized to web-based education that included a review of personalized treatment history and risk for late effects did not demonstrate improved knowledge compared with those who received physician-centered education. In this study, utilization of the web-based platform was quite low, suggesting that survivors are less engaged when online material is limited to the SCP. Despite these concerns, other studies have shown that young survivors are interested in adoption of ePHRs, as well as access to online social support, education, and opportunities for patient-to-patient interaction as part of their survivorship care.[63,64] There is evidence that integration of complementary online tools and features, such as the efforts now underway to further enhance the PFC Survivor website, may entice survivors to take full advantage of this platform, enhancing the delivery of educational content and minimizing user attrition.
Web-based systems for survivorship care have additional limitations, one of which is the amount of time required upfront to input the data on diagnosis and treatment. Most clinics leveraging web-based systems that rely on provider entry report use of dedicated personnel who enter data in advance of the survivor clinic visit. However, countries with well-annotated cancer registries have the distinct advantage of being able to pull verified data from those registries, so only minimal input is needed from oncology providers to generate a comprehensive SCP. Data from the Colorado Central Cancer Registry have similarly been linked to a web-based system and used to generate treatment summaries through an online survivorship module. Other systems have investigated strategies that interface with the electronic medical record, permitting autopopulation of treatment-related information. Efforts such as these reduce the potential concern for errors in survivor treatment history data that may occur when data are entered without subsequent verification.
Another notable limitation to web-based systems is the reported user demographics. Only one of the previously described tools is available in both English and Spanish, and none are available in other languages. Also, internet-based tools are more likely to be used among younger cancer survivors with higher educational levels and socioeconomic status,[68,69] hindering access for older or socioeconomically disadvantaged populations who may be at higher risk for suboptimal survivorship care.
Finally, there are potential concerns regarding data security with both local and centralized Cloud-based storage of electronic protected health information (ePHI). Regardless of where data are stored, the responsibility of keeping ePHI both secure and private should be shared between the hosting site and the developers of these web-based platforms. As recommended by HIPAA, such relationships should include a business associate agreement, which is a contract between the HIPAA-covered entity and a HIPAA business associate that restricts access to ePHI in accordance with HIPAA guidelines. Further, as required by the HIPAA Security Rule, all covered entities should create a disaster recovery plan that specifies the resources, actions, personnel, and data that require protection, as well as a strategy for reinstating health information in the event of a natural disaster or system failure. Thus, while centralized storage of medical and patient information in Cloud infrastructures can meaningfully improve access to care, just as for data that are stored locally, it is critical that all covered entities adhere to HIPAA recommendations for maximizing data security.
The societal impact of effective long-term follow-up care for the growing population of childhood cancer survivors cannot be underestimated. Survivors who regularly engage in follow-up care are more knowledgeable about their health risks and have better health outcomes than those who do not seek routine care. Improved adherence to the COG LTFU Guidelines may minimize or even prevent well-described late effects of cancer treatment—the objective of important future research. Web-based systems designed to support survivors and their medical providers complement the enormous strides made in development and maintenance of survivorship guidelines, and are expected to broaden accessibility to these guidelines and facilitate their translation into clinical practice.
Financial Disclosure: The authors have no significant financial interest in or other relationship with the manufacturer of any product or provider of any service mentioned in this article.
Acknowledgments: The authors thank our colleagues from the Childhood Cancer Survivor Clinic at the University of Texas MD Anderson Cancer Center, Cook Children’s Medical Center, Driscoll Children’s Cancer and Blood Disorders Center, El Paso Children’s Hospital Outpatient Clinic, the Texas Oncology Pediatric Hematology and Oncology Program, Vannie E. Cook Jr Children’s Cancer and Hematology Clinic, Dell Children’s Blood and Cancer Center, and the Greehey Children’s Cancer Research Institute for their support and participation in the launch of the PFC Survivor website. We would also like to acknowledge the survivors of childhood cancer and their families who have participated in research and related efforts to improve survivorship care. Passport for Care is funded by the Cancer Prevention Research Institute of Texas (under grant numbers PP130070, PP100090, and PP170036, to principal investigator David G. Poplack, MD).
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