This modified Delphi study convened a panel of experts in biomedical ethics and reached consensus that the principles of beneficence, non-maleficence, and autonomy are related to our previously proposed definitions of over- and undertreatment in older adults with cancer. The panel also reached consensus that, in most cases, it is unethical to make a treatment recommendation without (1) formal assessment of patient frailty (e.g., via a geriatric assessment) and (2) the opportunity for a patient to share their values, goals, and/or preferences. The panel did not reach consensus regarding the relationship between justice and over-/undertreatment; however, the panel concluded that justice applies to undertreatment when an oncologist withholds potentially beneficial cancer treatment in an older patient based on their age alone.
Tensions among bioethical principles can lead to over- and undertreatment in older adults with cancer (Table 5). With near unanimous agreement on the first round, the panel reached consensus that valuing the principle of beneficence over nonmaleficence can lead to overtreatment. This overemphasis on beneficence stems from biomedical reductionism, focusing more on the cancer-centric benefits of treatment rather than the impact of a treatment on the whole patient [14]. The panel agreed that the criteria of our definition of overtreatment appropriately elevated the overlooked principle of nonmaleficence. The concept of “minimizing harm” in older patients—especially those who are frail—must be weighed equally alongside “maximizing benefit” in terms of cancer control [2].
The panel reached consensus that overtreatment can also occur when oncologists prescribe cancer treatment out of a belief they are adhering to their specialty’s professional ethics, even when there is no evidence regarding treatment effects in older patients, or when existing evidence suggests that harms outweigh benefits. Providing a less intensive treatment option—including different drugs, reduced dosing, reduced frequency, or no treatment altogether—may be seen as failing to uphold a professional duty to provide patients treatment options that maximize cancer control [15, 16]. Oncologists may therefore view that cancer recurrence or progression in an older patient prescribed a less intensive treatment option poses a greater risk than the increased toxicity resulting from a more intensive treatment option. This calculus in decision-making has even been called the “Oncologist’s Wager”, an allusion to the historical “Pascal’s Wager” that concluded that the severity of the potential negative consequences of not pursuing an action (in the case of oncology, cancer spreading or recurring after a recommendation for less intensive or no treatment) were always greater than the potential negative consequences of pursuing an action (in oncology, toxicity after a recommendation to treat cancer) [17]. One implication of our findings is that by reasserting the principle of nonmaleficence alongside the principle of beneficence, oncologists will better adhere to their specialty’s professional ethics when they acknowledge that a given treatment’s harms may outweigh its benefits in frail older patients. In these scenarios, prescribing a less intensive treatment is not a form of undertreatment, but rather an ethically appropriate recommendation that prevents overtreatment.
The panel also reached consensus that tensions between autonomy and other principles can lead to both overtreatment and undertreatment. When nonmaleficence overrides autonomy, undertreatment can occur if an oncologist presumes that an older adult would not accept the risks of cancer treatment without first clarifying patient goals and preferences. When beneficence overrides autonomy, overtreatment can occur if an oncologist presumes the potential benefits of cancer treatment are desirable and prescribes treatment without clarifying goals and preferences. As reinforced by the panel, an older adult has the right to decline a treatment even when the oncologist believes it is of benefit. In this scenario, considering a less intensive option, or no cancer treatment at all, is not a form of undertreatment, but rather an ethically appropriate recommendation that respects patient autonomy.
Conversely, when autonomy overrides nonmaleficence, overtreatment can occur if an oncologist appeases the desire of an older patient (or patient’s family) to receive an intensive cancer treatment, despite the oncologist’s concern that the treatment’s harms likely outweigh its benefits. The overemphasis on preserving patient autonomy in modern medicine has even been referred to as the “tyranny of autonomy”; respecting patient preferences does not imply elevating their superiority in all cases above oncologists’ expertise [18]. Even if an older patient (or their family) requests an intensive treatment option, an oncologist’s recommendation for a less intensive alternative respects both autonomy and nonmaleficence if the oncologist believes the alternative to be a safer option that provides a benefit better aligned with the patient’s stated goals.
Regarding justice, the panel concluded that withholding a guideline-recommended therapy based on age alone exemplifies a lack of justice. Our definitions of over-/undertreatment advocate for the use of fitness/frailty when evaluating benefits and harms of treatments in older adults, avoiding arbitrary cutoffs based solely on chronologic age [19]. The panel’s inability to reach consensus on relating our definitions to the principle of justice as a whole stems from justice’s inherent call to consider other patients in the healthcare system when making individual-level treatment decisions (Supplemental Figure 3). This aspect of justice stands in contrast to autonomy, beneficence, and nonmaleficence, which are more readily applied to decisions in individual patients. Nonetheless, the virtual discussion session provided insight into how overtreatment of older adults unlikely to benefit from an intensive regimen may lead to undertreatment of other patients in the healthcare system (Supplemental Figure 3B). Moreover, if an older adult who could benefit from cancer treatment cannot access it due to mobility or functional limitations, geographic distance, or unreliable transportation, this lack of access reflects system-level inequalities that contribute to undertreatment (Supplemental Figure 3A) [20]. The same applies to an older adult unable to access a geriatric assessment and interventions that in turn leads to suboptimal cancer treatment [21].
Leading cancer organizations such as the American Society of Clinical Oncology (ASCO) now recommend formal assessment of frailty, by way of a geriatric assessment in older adults undergoing systemic cancer treatment [22, 23]. Our panel concluded that, in most cases, prescribing cancer treatment without frailty assessment raises ethical concerns. Frailty assessment shifts a cancer-centric view of treatment effects to a more holistic, patient-centered view, one that considers whether treatment benefits and harms differ in frail older adults compared to the fitter and/or younger patients who are overrepresented in clinical trials [24]. Evaluation of benefits and harms in light of an older adult’s physiology mitigates the risk of making treatment decisions based on age alone, which violates justice. This shift to a more patient-centered evaluation of benefits and harms also resolves the tension between beneficence and nonmaleficence, since it encourages weighing the tumor-specific benefits of treatment against the risk of treatment toxicity [25, 26]. At the same time, simply labeling a patient as “frail” (e.g., from gestalt and not after formal geriatric assessment) and withholding guideline-based treatments solely on that basis can reflect undertreatment—just as it can when decisions are based only on chronological age. This is especially problematic when a treatable cancer is the main cause of a patient’s frailty, or when addressing other frailty factors could improve tolerance to beneficial cancer therapies [27].
In this vein, a more patient-centered evaluation via formal frailty assessment reveals other health deficits (e.g., comorbidities, cognitive impairment, or functional limitations) that often present concurrently with cancer in older patients. Our definition of undertreatment includes the failure to recognize and optimize these nononcologic health deficits, since their optimization can mitigate toxicity risk and promote adherence to cancer treatment [28]. Recent randomized controlled trials conclude that oncology care that is guided by frailty assessment (compared to standard oncology care) informs anti-cancer treatment modifications and/or supportive care interventions that mitigate overtreatment of an older adult’s cancer and undertreatment of their nononcologic conditions [29,30,31]. Evidence from trials is more limited regarding the effectiveness of frailty assessment in improving long-term survival, as the survival outcomes are assessed at 6-month and 12-month endpoints in the large RCTs. Also, caution should be exercised against reflexive treatment de-escalation simply because a patient has one or more health deficits found on geriatric assessment. Geriatric assessment is meant to augment and improve clinical judgment, not supersede it. Just as withholding guideline-recommended treatments based only on labeling a patient as “frail” can reflect undertreatment, withholding guideline treatments based only on the presence of functional or cognitive deficits may also reflect undertreatment, especially if the patient prioritizes life prolongation above other outcomes.
Moreover, identifying and addressing deficits such as hearing and/or cognitive impairment early in the treatment decision process can also better ensure that oncology teams deliver fair and informed communication. Evaluating deficits includes considering the ability of the older patient to receive information on treatment decisions, to weigh risks and benefits of different options, and to ascertain his/her overall capacity to accept or reject a treatment recommendation. Indeed, formal frailty assessment has been shown to (1) raise awareness of aging-related concerns among oncologists and (2) improve their communication with older patients and caregivers [32, 33]. Since the way in which an oncologist presents different treatment options plays a determining role in the final treatment decision, a formal frailty assessment of health domains essential to older adult well-being expands a cancer-centric discussion to a more patient-centered discussion.
The panel also reached unanimous consensus that, in most cases, it is unethical to prescribe cancer treatment without first offering older patients the opportunity to share their goals and preferences. Whereas some older patients prioritize cancer control just as much as younger patients, other older adults prioritize maintaining independence and avoiding time spent in the hospital [34]. In the latter case, aggressive treatments may present more harm than benefit if their side effects jeopardize function and quality of life—even if the treatments lengthen life [35]. Evidence suggests that there is often inadequate communication regarding goals of care between patients, families, and oncologists, undermining autonomy and potentially contributing to over-/undertreatment [36,37,38]. Multiple interventions have been tested to improve goals of care communication in oncology, such as decision aids and communication training for oncologists [39, 40]. Our findings underscore the importance of these efforts, particularly in older patients for whom benefits of intensive therapy have not been established. Our proposed criteria of over-/undertreatment require defining the “benefits” older adults wish to pursue and the “harms” they wish to avoid. Obtaining these goals and preferences reasserts respect for patient autonomy, resolving tensions between this principle and others.
There are limitations to this study. First, we did not explore other ethical frameworks that may apply to our definitions of over-/undertreatment. We focused on the Beauchamp and Childress principles that are the most widely taught and recognized frameworks among the medical community. Although the tensions that can arise among these ethical principles are often cited as a limitation for their use in guiding treatment decisions, our work reveals that identifying these tensions can better explain how over- and undertreatment occurs. Second, our Delphi panel consisted of experts in biomedical ethics from North American institutions. Lack of representation outside of North America may influence the generalizability of our findings, and different countries and cultures may vary the application of ethical principles to decision-making in older patients. Finally, the very attempt to apply ethical standards to better define over- or undertreatment in older adults may appear problematic, since the benefits and harms of novel treatments in older adults are often uncertain. However, treatment decisions must still be made despite this uncertainty, and the lack of evidence to guide such decisions necessitates adherence to bioethics.
In conclusion, this work establishes the ethical principles underlying over-/undertreatment in older adults with cancer. The identification of relevant tensions among these principles is a vital step towards reducing over-/undertreatment, ensuring older patients receive appropriate care when facing limited evidence. Our findings suggest an ethical imperative to scale formal assessment of frailty via the geriatric assessment for more widespread use in oncology practice, as well as evaluation of patient goals and preferences.