Abstract: The number of US cancer survivors has increased from fewer than 4 million in the 1970s to 18.1 million in 2022, with the increase reflecting advancements in screening, diagnosis, treatment, and supportive care. Despite these advancements, cancer remains the second leading cause of death in the United States. Survivors face a myriad of health concerns, including residual effects of treatment, psychological issues like distress and depression, and an elevated risk of secondary cancers. This article highlights the need for long-term surveillance and a multidisciplinary approach to care, emphasizing the importance of personalized health plans and regular monitoring. It also discusses the challenges encountered in addressing fatigue, sexual health, and disparities in outcomes that negatively affect minorities and financially disadvantaged persons. The article concludes by describing different models of care and the role of primary care providers in managing survivorship care and advocating for a shared-care model to improve access to and integration of care.
Introduction
The emergence of cancer survivorship care as a discipline reflects one of medicine’s greatest triumphs, yet it also exposes some of our most significant challenges in health care. Of note, the number of cancer survivors has increased from just under 4 million in the 1970s to 18.1 million in 2022.1 This trend reflects an increasingly aging population of patients who are at elevated risk for cancer, along with improvements in screening, diagnosis, treatment, and supportive care. The improved cancer numbers also reflect salutary changes in the American diet and lifestyle (more healthful diet, decreased smoking rates). Cancer remains the second leading cause of death in the United States.2 Patients now have access to better screening and better therapies; however, cancer survivors represent a broad array of diagnoses, therapies, and treatment plans. Patients can have many health concerns, and these may include the residual effects of cancer treatment, which can be surgical, medical, or hormonal. Often, patients require but do not have ongoing access to a team of care providers. After cancer treatment ends, patients must frequently undergo surveillance not just for the initial cancer diagnosis but also for cancers and other disorders that can arise from treatment. Our current health care system has struggled to respond to this complex set of needs. In many cases, no single defined pathway for survivors exists, and the ideal path can be difficult to discern and implement.
Perhaps a good starting place to look at survivorship is a 2006 consensus report from the Institute of Medicine: “From Cancer Patient to Cancer Survivor: Lost in Transition.” The report noted, “Cancer survivors swell the ranks of the many places where we live, work, and play, yet, as our committee concluded, they remain largely understudied and lost to follow-up by our scientific research and health services delivery communities, respectively.” A major cause of the relatively slow pace of progress is the lack of long-term studies on the effects of cancer treatment, including the psychological and economic challenges faced by survivors. Another factor is the disconnect between medical research and practical treatments.3 Although scientific advances in cancer biology have been significant, the process of translating these discoveries into effective treatments for survivors has been relatively slow.4
This article explores the current state of cancer survivorship and highlights some of the progress that has been made, specifically by examining the unique concerns faced by this growing population.
Unique Health Concerns in Survivors
Cancer survivors require long-term surveillance that can last a lifetime. Health care for patients living with or recovering from cancer is complex and includes the effects of both the diagnosis and the treatment. Survivors are at elevated risk for psychological, physical, and financial problems. Psychological issues can be triggered or exacerbated at any point following a cancer diagnosis. Distress, anxiety, and depression are the most common mental health ailments seen in this population. As for who is most at risk, a large study of more than 117,000 adult cancer survivors found that diagnosis at a young age, fair or poor health status, and a history of illicit drug use were associated with an increased risk of negative mental health outcomes. Financial stressors, the fear of recurrence, the development of secondary cancers, and the fear of death and a shortened lifespan may also increase the likelihood of poor mental health outcomes.
Distress
Many cancer survivors experience distress, which is an emotional state during which a person’s failure to adapt or respond to difficult situations leads to maladaptive behavior. Distress is often driven by fear of disease progression but can also be driven by weakness, pain, or poor sleep.5 It can range from mild to severe, and in some cases inpatient management is required. Validated tools are available to measure distress. The recommendation from the National Comprehensive Cancer Network (NCCN) in 1999 was to screen all cancer survivors for distress with a tool known as the Distress Thermometer (Figure). The Distress Thermometer includes a self-reported distress level and a list of self-identified problems that can guide clinicians in the use of supportive measures as needed. Distress during the preceding 7 days is measured on a scale from 0 (no distress) to 10 (extreme distress). Results obtained with this screening tool can help the provider determine the need for further evaluation and treatment.
However, this is not a perfect test, and the definition of distress in this context may need to be clarified for patients. Also, providers may be quick to refer a patient to psychological or social services without a clear understanding of the patient’s preference for the next steps. Conversely, missing the opportunity to acknowledge and discuss distress when it is present can also be harmful. Lack of time, limited availability of resources, and lack of comfort or knowledge in discussing the results of the Distress Thermometer screen are barriers to best care.
Depression
Depression is different from distress and is a common concern among cancer survivors, whose risk of significant illness is much higher than that of the general population. Although studies have shown differing results, estimates of the rates of depression in patients with cancer range from 5% to 25%. It can be challenging to distinguish among symptoms such as fatigue, lack of concentration, and slowed cognitive responses in patients with cancer, as these can result from the cancer itself or from current or previous treatment. It is therefore not surprising that depression often goes undiagnosed.6
Validated screening tools are available to assess the risk for depression. The Patient Health Questionnaire (PHQ 2/9) screening tool, which is validated to screen for depression in patients with cancer, has a sensitivity of 83% and a specificity of 92%.7
In contrast to the prevalence of depression in the general population, which is higher in women than in men, in patients with cancer it is equal in men and women. Also, depression in these patients more often manifests as somatic symptoms than as feelings of sadness or suicidal ideation.8 Somatic symptoms that can hinder normal functioning include aches and pains, poor sleep, and fatigue. The risk of depression varies considerably with the type of cancer. Survivors of head and neck cancer have a 40% to 50% risk of experiencing depressive symptoms,9 whereas survivors of testicular cancer have a 7.5% risk of significant depressive symptoms.10 Patients with positive screening results should be referred to a health professional for further evaluation and treatment.
Cancer survivors need to be screened for depression routinely, including at times of recurrence or changes in staging for the worse. Regular screening increases the likelihood of a prompt diagnosis. Cancer survivors tend to have more physical complaints than other patients do, and clinicians should have a high index of suspicion for comorbid depression in patients who have somatic complaints. Ideally, cancer survivors with significant depression would receive care from a multidisciplinary team that includes an oncologist, a primary care provider, and a mental health specialist.
Fatigue
Cancer-related fatigue is characterized by an overwhelming, persistent sense of tiredness, exhaustion, and weakness that is not relieved by rest, is out of proportion to the level of activity, and interferes with daily quality of life.11 Because fatigue can affect up to 50% of all cancer survivors and up to 75% of patients with metastatic disease, clinicians should routinely screen for fatigue in all cancer survivors. Despite its prevalence, fatigue is underdiagnosed and undertreated. First, patients may be hesitant to complain about fatigue for fear of not receiving the maximum treatment or of being labeled as difficult, or because they fear that fatigue is a sign of advancing disease. Conversely, providers may be hesitant to ask about fatigue owing to a lack of confidence about evaluation and concern that treatment may require more investigation than the allotted time for the clinical appointment allows.
The etiology of fatigue in cancer survivors is often multifactorial. Fatigue can be caused by cancer itself, chronic pain, emotional factors like depression and anxiety, sleep disturbances, nutritional deficiencies, medications, hormonal imbalances, activity level, or stress. The European Organization for Research and Treatment of Cancer Core Quality of Life Questionnaire (EORTC QLQ-C30), which is a 10-minute tool designed to help identify the presence of cancer-related fatigue, carries a Level A strength of recommendation.12 When the amount of time to address fatigue is limited, good questions include the following:
1. Severity: On a scale of 1 to 10, how would you rate your fatigue over the past week?
2. Duration: Have you experienced persistent fatigue in the last 2 weeks?
3. Impact: Does your fatigue interfere with your ability to perform daily activities?
Addressing fatigue begins with a comprehensive history, including a review of the issues listed in the reason for the visit and a detailed physical examination. Depending on the findings, supportive laboratory testing could include a comprehensive metabolic panel, complete blood cell count, and thyroid-stimulating hormone measurement, with the type of cancer, type of chemotherapy, and site and duration of radiotherapy when appropriate considered to aid decision making. For both providers and patients, the workup can be long and the results inconclusive. Visit length does not always take into account the time needed to address fatigue adequately, especially when a patient has multiple competing issues. Setting an agenda at the beginning of a visit can help make the best use of time during a visit.
The American Society of Clinical Oncology (ASCO) recently updated its guidelines for managing fatigue in adult patients with cancer. On the basis of evidence of moderate quality, ASCO concluded that cognitive behavioral therapy, exercise, mindfulness exercises, tai chi, and qigong are the most effective interventions.13 These activities can be pursued both during and after treatment and tailored to according to the patient’s interest and fitness level. Yoga and acupressure received weaker recommendations, and the guidelines recommended that psychostimulants such as modafinil and armodafinil not be used to relieve cancer-related fatigue.
Secondary Cancers
Cancer survivors have a higher risk of subsequent cancers, for several reasons. First, some cancer treatments, such as radiation and certain chemotherapy agents, can damage healthy tissue and increase the risk of cancer-causing mutations. Additionally, inherited mutations in genes such as BRCA1 and BRCA2 increase the risk of more than one type of cancer. Furthermore, some exposures increase the risk of multiple cancers. Infection with human papillomavirus, for example, increases the risk for both cervical cancer and throat cancer.
Once patients have completed the treatment of their primary cancer, survivors have approximately a 10% increased risk of death due to a secondary cancer later in life.14 In long-term survivorship care, the first step in addressing this risk is knowing some basic facts about the patient’s cancer history and subsequent treatment modalities. Survivors whose cancer has a heritable component also should be asked to update their family history of cancer regularly. Smoking and obesity play a significant role in increasing patients’ risk for secondary cancers, so these issues warrant routine management as well. Many validated tools are available to help patients quit smoking, including behavioral therapy, cognitive therapy, motivational interviewing, counseling, medications, and nicotine replacement therapies,15 but patients must be ready to quit. Providers and patients must work together to find the best strategy for getting smokers to quit, with the understanding that relapse is common.
The good news, according to a quality improvement initiative report from the American College of Surgeons Commission on Cancer, is that nearly 90% of programs routinely ask about smoking status and document tobacco use among survivors.16 The report indicates that screening for tobacco use is now standard practice in most cancer centers. Additionally, ASCO and the NCCN recommend that all cancer survivors who use tobacco be offered both behavioral and pharmacologic cessation support as standard of care.17 The cost of the program to the patient can range from nothing to $2000, depending on the program’s intensity and funding mechanisms.18 Smoking cessation produces survival benefits and, therefore, should be encouraged whenever possible.
Chemotherapy, radiation therapy, and hormonal therapy have all contributed to an increased survival rate, but they also can put patients at increased risk for late effects and secondary cancers. Late effects such as weight gain (from long-term corticosteroid use), joint pain (from androgen deprivation and estrogen-blocking agents), and fatigue can make exercise difficult.
Sexual Health
Sexual health is often adversely affected by a cancer diagnosis and subsequent therapies. Reduced sexual function can be a significant concern that worsens over time.19 Nonetheless, many patients are reluctant to initiate discussions of sexual health with their clinician. In one study, women who reported the lowest sexual health scores on a screening test had not raised their concerns independently.20 Providers may not address the sexual problems of their patients adequately owing to time constraints, fear and embarrassment, or outdated information. For example, physicians may be reticent to prescribe vaginal estrogen—which can improve sexual function and decrease the risk of urinary tract infections—because the package insert long stated that it is contraindicated in breast cancer survivors. Observational studies, however, have found no link between vaginal estrogen and an increase in breast cancer recurrence.21
In addition to patients with prostate or breast cancer, many others would benefit from counseling regarding sexual function ahead of therapy. For example, patients with colon cancer have a 40% to 80% chance of experiencing significant sexual side effects following treatment,22 and survivors of head and neck cancer have a 60% to 80% chance of sexual dysfunction after treatment. It is critical to look beyond the cancers that are generally thought of when counseling ahead of therapy is being considered.23
Clinicians need to be able to address sexual concerns with patients in a way that normalizes the experience. Ideal care for cancer survivors would include physical, psychological, and relational aspects. Additionally, in the context of loss of sexual function, clinicians will recognize grief and mourning as part of the recovery process and support their patients. When possible, patients should include their partners in sexual health counseling if both agree to the experience,24 and when possible, they should have access to and be offered sexual health counseling to assist them in working through these challenges.
Chronic Disease and Cancer Survivorship
It may be a surprise that in the case of many common cancers, including prostate cancer, patients are less likely to die of the cancer than of another cause. Although prostate cancer is diagnosed 1 in 9 men in their lifetime, only 1 in 44 ultimately die of prostate cancer; the 5-year survival rate of individuals with localized prostate cancer is greater than 99%.25 Strikingly, 45% of men who have prostate cancer die of something other than the cancer.26 The same is true for breast cancer, which affects roughly 1 in 8 women but carries a mortality risk of just 1 in 40.27 These gaps reflect the fact that most cancer patients die of other causes. Cancer survivors are more likely than the rest of the population to be affected by multiple chronic conditions and have an elevated risk of hypertension, diabetes, kidney disease, liver disease, heart disease, and chronic obstructive pulmonary disease.28
In Search of an Ideal Care Model for Cancer Survivors
Keeping up with and staying on top of cancer care can be challenging in the best of circumstances. As previously mentioned, cancer in its many forms can entail diverse sets of treatments and subsequent medical, psychological, and sexual side effects. A lot of information must be communicated to and processed by the patient. Visit times are often inadequate to cover all questions, and it can be difficult for patients to remember everything that is discussed. A good way to assess patient comprehension is to ask patients about their current understanding of their cancer and care plan. Open-ended questions can allow the provider and patient to create a shared mental framework to prioritize discussions. By asking patients what questions they have before moving on to the next steps, especially when a setback has occurred or a new finding has come to light, clinicians can quickly gauge patient preparedness for future discussions.29
ASCO has published tools to aid clinicians in providing survivorship care in these cases. One such tool is a summary of the patient’s diagnosis and treatment, familial cancer risk, recommended surveillance, anticipated or possible long-term sequelae of treatment, and anticipatory guidance.30 This tool equips providers with the information needed to monitor patients in the ambulatory care setting. Survivorship care plans embedded in electronic medical records have attempted to improve communication with clinical decision systems; however, these have shown limitations in terms of collecting data, defining roles, designing documents that adapt with time, allowing multiple providers to add their input, categorizing patient risk, and compiling a list of the individual patient’s treatment and potential needs. It can be challenging to define and communicate the roles of each team member clearly, and health systems have struggled with how best to summarize and share information when following the Institute of Medicine recommendation to use survivorship care plans.
Data demonstrating the effectiveness of any of these survivorship care plans have not been robust. The plans have not consistently been shown to improve patient-reported outcomes regarding quality of life, psychological well-being, or satisfaction with care.31 However, they do have a positive effect on proximal outcomes. They improve the amount and clarity of information survivors receive, enhance the coordination of care, and can increase adherence to recommended follow-up care—especially when they are delivered in conjunction with counseling or behavioral interventions.32 The most effective components and delivery methods combine survivorship care plans with active counseling or communication interventions rather than using the plans alone. Various team structures have been established to address some of the challenges associated with providing the best care for cancer survivors. The other models aim to improve access for all survivor populations, increase the capacity of oncologists to care for patients with new cancer diagnoses, enhance the ability of the cancer team to monitor the long-term effects of treatment and secondary cancers, and improve integration with primary care. Some models are spearheaded by the oncology team and emphasize communication with the primary care team; these may include a general survivorship clinic, a multidisciplinary survivorship clinic, or a disease- or treatment-specific survivorship clinic.
One model that can empower the primary care provider is the shared-care survivorship model, in which the primary care physician takes over a patient’s survivorship care in addition to general health maintenance within 2 years of completion of the patient’s therapy. In this model, the oncologist can serve as a consultant for any questions or concerns. Referral back to the oncologist would be indicated if evidence of recurrence is noted. One study proposed using a risk-stratified version of the shared-care survivorship model, in which the degree of longer-term oncology involvement would be based on the risk of side effects or recurrence.33 One of the challenges of integrating primary care providers into survivorship care is the lack of survivorship knowledge. ASCO has created a table of core competencies in survivorship care in which primary care providers are expected to be proficient.34
At its most basic level, regardless of the model, ideal survivorship cancer care should include the following: a personalized health plan that the patient can access and understand; access to a well-trained multidisciplinary group of clinicians who are able to monitor the patient regularly for cancer recurrence, secondary cancers, and known late effects of treatment; and access to mental health counseling and financial support services if needed.
Diet and Exercise During Survivorship
A balanced diet contributes to overall health, but only a few large randomized controlled trials have looked at the effects of diet on meaningful clinical cancer outcomes. Data are limited on the effects of dietary recommendations—including increased fruit, vegetable, and fiber intake—on life expectancy after a cancer diagnosis.35 We have seen some limited data on selected cancers indicating improved outcomes with a plant-based diet, but currently, data to support any specific diet are weak and incomplete. However, the American Cancer Society (ACS) does offer some basic recommendations. First, a registered dietitian should evaluate patients at risk for malnutrition.36 Second, patients should strive to maintain a healthy weight.37 Finally, if a patient is not able to maintain adequate nutritional support despite maximal effort at any time in their cancer journey, it is appropriate to consider enteral or tube feeding. When enteral feeding is not possible, parenteral feeding should be considered. The NCCN offers a few basic guidelines for healthy eating for all cancer survivors:
• Maintain a healthy diet, with adequate macronutrient and micronutrient content from both animal- and plant-based food options but with a preference for plant-based foods.
• Exercise caution regarding the overuse and misuse of dietary supplements during and after treatment.
• Adhere to food safety procedures to avoid foodborne illnesses.38
A growing body of evidence supports the use of physical activity “prescriptions” in the management of several cancers, cancer-related symptoms of depression, physical dysfunction, and anxiety. In fact, a recent pan-cancer analysis of exercise vs no exercise after diagnosis found a 25% reduction in all-cause mortality.39 The benefits varied across cancers and suggested that more research should be undertaken in this area. Nonetheless, patients are encouraged to be active participants in their physical activity care plan and to communicate their goals, preferences, and limitations. Doing so will help to ensure and align specific, obtainable, and measurable physical activity goals. The ACS guidelines provide further information on diet and physical activity after a diagnosis of several common cancers.37
Ongoing Inequities
Although a considerable amount of work has been done to improve the experience of cancer survivors, outcomes in minority groups and persons who are financially40 disadvantaged continue to be relatively poor. The outcomes of historically marginalized racial and ethnic groups are worse than those of non-Hispanic cancer survivors. Patients who report racism also report poorer health, which carries over into cancer survivorship care.41 A recent review article summarizing the state of cancer occurrence and outcomes in rural areas of the United States confirmed that certain racial and ethnic groups tend to have a higher cancer burden, a lower level of cancer-related knowledge, and lower rates of cancer screening than do non-Hispanic Whites living in the same rural areas. Additionally, patients belonging to marginalized racial and ethnic groups who undergo monitoring for cancer in rural areas have a higher incidence of cancer and higher mortality rates in comparison with their White counterparts.42
Opportunities for Advanced Training
Given the significant rise in the number of cancer survivors in the United States, cancer survivorship training programs have been developed at leading cancer centers to better equip clinicians with the knowledge and skills necessary to address the complex needs of cancer survivors across the care continuum. These programs, which typically cover key domains identified by the Institute of Medicine and are reinforced by ASCO and the ACS, include surveillance for recurrence, management of late and long-term effects, health promotion, psychosocial support, and coordination of care between oncology and primary care providers.43
Summary
Survivorship care should begin at the time of diagnosis. Patients are best served when survivorship care is integrated into their overall health care, with any other medical problems factored in. Routinely screening for depression and anxiety in cancer survivors and having a system in place for counseling and treatment is beneficial and can help patients manage the stressors that can accompany a cancer diagnosis more effectively.
Disclosures
Dr Ragsdale has done consulting for Merck, Dr Oeffinger is the co-founder and chief clinical officer of Maia Oncology, and Dr Rousseau has no disclosures.
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