More than 25 years ago, Dr Fitzhugh Mullan described the seasons of survival in a narrative of his personal experience of being diagnosed and treated for cancer and facing the other side of the stethoscope in the New England Journal of Medicine in 1985.1 His description of cancer survivorship included an individual’s experience across the cancer continuum, from initial diagnosis through the remainder of life. “It was desperate days of nausea and depression. It was the elation at the birth of a daughter in the midst of treatment. It was the anxiety of my monthly chest xrays.… It was survival, an absolutely predictable but ill-defined condition that all cancer patients pass through as they struggle with their illness.”1
“Seasons of Survival” was also one of the first articles to describe the natural history of cancer survivorship. That paradigm included 3 phases (Figure 1).1 During the past 3 decades, however, seminal advances in cancer detection and treatment have evolved. Improved understanding of cancer biology and molecular profiling of patients’ tumors has led to more targeted therapy. The 5-year survival rate of adult cancer patients is growing steadily and currently is estimated at 64%.2 And the number of cancer survivors grows constantly, increasing from 3 million in 1971 to an estimated 11.7 million in 2007 (Figure 2).3 By 2020, it is estimated that there will be 20 million cancer survivors in the United States.
Improvements in long-term survival rates vary significantly among cancer types. Survival rates of patients with chronic myelogenous leukemia (CML) have improved dramatically because of highly effective treatment, leading to a growing number of survivors living in remission. Survival rates have improved somewhat less in breast cancer and even less in lung cancer (Figure 3).4 In total, however, the number of cancer survivors who live beyond 5 years also has increased (Figure 4).4
A NEW PARADIGM
In light of the growing number of cancer survivors and the practical issues of healthcare delivery, we propose a revision in the seasons of survival paradigm (Figure 5). The survivorship trajectory for individual cancer survivors is quite variable, and the transitions may occur at different intervals. In addition, as some survivors develop secondary malignancies, they essentially reenter acute survivorship. End of life also is encompassed within the cancer survivorship experience.
Many emotional aspects of the acute period of cancer diagnosis and treatment have not changed significantly in the past 25 years; although new drugs, dose intensity, and dose density have added new toxicities. Supportive care has been improved greatly, however.
The title of the Institute of Medicine’s 2005 report, From Cancer Patient to Cancer Survivor: Lost in Transition, aptly describes what for many is a difficult transition back to “normal” or a “new normal.”5
Extended Cancer Survivorship
Mullan described extended survivorship as a period of watchful waiting and uncertainty about the future. Traditionally this was considered to be the 5-year period of observation after a cancer diagnosis. Now it is clear that the risk may drop off substantially before 5 years or may continue almost indefinitely.
A growing number of cancer survivors are living with cancer as a chronic disease. Patients with CML or gastrointestinal stromal tumors exemplify chronic cancer survivorship. Chronic survivorship also collectively refers to patients with metastatic disease who live with cancer for an extended time because of the introduction of newer agents and protocols.
Mullan characterized this season as a time when cancer survivors experience less fear and an increasing sense of permanency. This is a heterogeneous group, however: some are “cancer free and free of cancer,” whereas others are “cancer free but not free of cancer”—either physically or emotionally. Some cancer survivors reenter the acute phase of survivorship when diagnosed with a second cancer or a secondary cancer related to previous therapy.
Cancer Free and Free of Cancer.
Cancer survivors may be cured either surgically or by local or systemic therapy and live for many decades. Many do not experience late or long-term medical or emotional effects of the experience and cancer feels like a distant part of their past medical history.
Cancer Free But Not Free of Cancer.
Aziz and Rowland distinguished the term late effects as a group of unrecognized toxicities that are absent or subclinical at the end of therapy and become manifest later with the unmasking of potential injury due to any of the following factors: developmental processes; the failure of compensatory mechanisms with the passage of time; or organ senescence.6 In contrast, the term long-term effects refers to any side effects or complications of treatment that begin during treatment and continue after treatment has ceased.6 Some researchers classify cognitive problems, fatigue, lymphedema, and peripheral neuropathy as long-term effects; others classify them as late effects.7-10
Second Cancers and Secondary Cancers.
The number of patients who develop second cancers is increasing, estimated at 16% of the cancer incidents reported to the National Cancer Institute- Surveillance, Epidemiology and End Results program in 2004.11 Second cancers can reflect the late effect of therapy (ie, radiation, chemotherapy, hormonal therapy), the results of habitual behavior (eg, smoking, alcohol), host factors(ie, cancer syndromes), environmental determinants, and synergism between the risk factors.12
End of Life
End of life is part of cancer survivorship, either during acute survivorship if the cancer progresses despite treatment, after a survivor is living with cancer as a chronic survivor, after relapse from extended survivorship, or after some period as a permanent survivor. Although a great deal is known about end-of-life care for patients who have been treated actively for cancer, less is known about how the dying experience may be different or special for permanent cancer survivors and their caregivers after having faced the possibility of dying years or decades before.
IMPLICATIONS FOR PRACTICE
More than 25 years have passed since Mullan’s landmark article. The chance of living beyond acute cancer survivorship has increased as has the total number of permanent survivors. Recent data suggest quantitative and qualitative shifts in the composition of the prevalent population of cancer survivors. The revised paradigm for the seasons of survival presented here differs from the model proposed by Mullan, by recognizing the significant period of transition after the completion of treatment; the heterogeneity of permanent, long-term cancer survivors; and the growing group of patients in chronic survivorship who are living with cancer. Comprehension of the seasons of survival along with the individuality of survivors and their diversity of needs may enhance our ability to provide needs-based care for cancer survivors.
Care of cancer survivors includes attention to all seasons of survival.13,14 Surveillance for recurrence is important, as are treatment of cancer-related adverse events and other comorbidities, surveillance to detect second and secondary cancers, and education to optimize health and enhance quality of life. Potentially, reducing comorbidities may reduce the risk and severity of late or long-term effects on a survivor’s health.15
Cancer survivorship programs can impact cancer survivors during one or more of the seasons of survival. Although it may be difficult to try to serve all cancer survivors in each and every season of survivorship, because their needs for surveillance for disease recurrence differ, health education, health behavior improvement, and secondary prevention can benefit any cancer survivor. Survivorship programs have an opportunity to tailor the types of services they offer to cancer survivors during the different seasons of survival based on the perceived and expressed needs of their medical community and, more importantly, their patients.
- Mullan F. Seasons of survival: reflections of a physician with cancer. N Engl J Med. 1985;313:270-273.
- Oeffinger KC, McCabe MS. Models for delivering survivorship care. J Clin Oncol. 2006;24:5117-5124.
- Altekruse SF, Kosary CL, Krapcho M, et al. SEER Cancer Statistics Review, 1975-2007, National Cancer Institute. Bethesda, MD, http://seer.cancer.gov/csr/1975_2007/, based on November 2009 SEER data submission, posted to the SEER website, 2010.
- SEER Cancer Statistics Review, 1975-2007, National Cancer Institute. Bethesda, MD, http://seer.cancer.gov/csr/1975_2007/, based on November 2009 SEER data submission, posted to the SEER website, 2010.
- Hewitt M, Greenfield S, Stovall E, eds. From Cancer Patient to Cancer Survivor: Lost in Transition. Washington, DC: The National Academies Press; 2005.
- Aziz NM, Rowland JH. Trends and advances in cancer survivorship research: challenge and opportunity. Semin Radiat Oncol. 2003;13:248-266.
- Loescher LJ, Welch-McCaffrey D, Leigh SA, et al. Surviving adult cancers. Part 1: physiologic effects. Ann Intern Med. 1989;111:411-432.
- Welch-McCaffrey D, Hoffman B, Leigh SA, et al. Surviving adult cancers. Part 2: psychosocial implications. Ann Intern Med. 1989;111:517-524.
- Herold AH, Roetzheim RG. Cancer survivors. Prim Care. 1992;19:779-791.
- Marina N. Long-term survivors of childhood cancer. The medical consequences of cure. Pediatr Clin North Am. 1997;44:1021- 1042.
- Ries LAG, Melbert D, Krapcho M, et al; eds. SEER Cancer Statistics Review, 1975-2004, National Cancer Institute. Bethesda, MD, http://seer.cancer.gov/csr/1975_2004/, based on November 2006 SEER data submission, posted to the SEER website, 2007.
- Travis LB, Rabkin CS, Brown LM, et al. Cancer survivorship— genetic susceptibility and second primary cancers: research strategies and recommendations. J Natl Cancer Inst. 2006;98:15-25.
- Given LS, Black B, Lowry G, et al. Collaborating to conquer cancer: a comprehensive approach to cancer control. Cancer Causes Control. 2005;16(suppl 1):3-14.
- Pollack LA, Greer GE, Rowland JH, et al. Cancer survivorship: a new challenge in comprehensive cancer control. Cancer Causes Control. 2005;16(suppl 1):51-59.
- Aziz NM. Cancer survivorship research: state of knowledge, challenges and opportunities. Acta Oncol. 2007;46:417-432