Introduction

Approximately 70 % of deaths from cancer occur in patients aged 65 and over [1]. The majority of clinical research in cancer care, however, is conducted in younger patients [2], and this discrepancy creates uncertainty for oncologists in extrapolating available data to treat their older patients. Additionally, many outcomes that are of interest to older patients, such as functional impairment and independence, are not evaluated in traditional clinical trials [3].

Caring for an older individual with cancer requires knowledge and expertise in both oncologic and geriatric issues. However, the goals of these two disciplines vary significantly. Oncologists focus on assessment of cancer variables, such as tumor biology and stage, as well as the development of cancer-specific treatment plans. Geriatricians, on the other hand, assess physiologic age and functional status, with a focus on optimizing an individual’s independence. Integrating these two skill sets into one individualized care plan can improve outcomes for the older patient with cancer. Additionally, knowledge of geriatric-specific issues such as falls or cognitive impairment can help providers anticipate potential complications [4••] and intervene in order to minimize treatment-related toxicity [5].

The field of geriatric oncology has evolved as these two unique disciplines have been merged in an effort to focus research efforts in understanding the optimal approach to the treatment of older adults with cancer [6]. However, there are relatively few dual-trained geriatric oncologists, and even fewer clinics specifically devoted to geriatric oncology assessment, and therefore it is essential that oncologists are trained in the basic principles of geriatrics and that geriatricians are educated on cancer-specific considerations for GA and are empowered to address potential geriatric issues to optimize their patients’ cancer care.

Feasibility and Impact of Geriatric Assessment (GA) in the Oncology Setting

Geriatric oncologists endorse the use of GA as a tool in the development of treatment plans for older adults with cancer [7]. Prior research has demonstrated that it is feasible to incorporate a geriatric-focused assessment into routine oncology practice [8]. Hurria and colleagues developed a cancer-specific GA that consisted primarily of self-administered questionnaires addressing the various geriatric assessment domains [9]. They determined that 78 % of patients were able to complete the assessment without assistance and that the mean time to completion was 27 minutes. The vast majority of patients (90 %) were satisfied with the length of the questionnaire. The cancer-specific GA has also been shown to be a useful tool incorporated into clinical trials investigating new treatments for older adults with cancer [10].

Numerous studies have demonstrated that older patients with cancer frequently have impairments in GA domains. In a prospective multicenter trial, Hurria and colleagues found that 43 % of patients had impairment in instrumental activities of daily living (IADLs) [4••]. Multiple other studies have demonstrated similar rates of functional dependence [9, 11]. Cognitive impairments are also commonly detected. Data from various studies indicate that approximately 20 % of older patients with cancer screen positive for cognitive impairment [12, 13]. Several analyses from nationally representative population-based databases show that having a previous diagnosis of cancer is independently associated with functional impairment, geriatric syndromes, and frailty [14, 15].

It has been demonstrated that utilization of GA is able to provide information beyond traditional oncology performance measures [16]. Studies have also investigated the ability of the GA to predict chemotherapy toxicity [4••, 17••]. The Cancer and Aging Research Group (CARG) prospectively evaluated 500 patients with comprehensive geriatric assessment and identified 11 factors that were independently associated with chemotherapy toxicity [4••], which included advanced age (>72 years), gastrointestinal or genitourinary malignancy type, standard chemotherapy dosing, polychemotherapy regimen, anemia, renal insufficiency, hearing impairment, history of falls, needing assistance with administration of medication, limited ability to walk one block, and decrease in social activities due to health status. A risk stratification tool was developed that was predictive of chemotherapy toxicity, and this model was found to be superior to the Karnofsky index of performance status, the existing standard used by oncologists to assess fitness.

Similarly, the Chemotherapy Risk Assessment Scale for High-Age Patients (CRASH) model was developed to predict severe hematologic and non-hematologic toxicity [17••]. The model was constructed and validated in a study of over 500 patients aged 70 and older with cancer, in which the authors determined that 64 % of patients experienced severe treatment-related toxicity. Geriatric-specific predictors of toxicity in the CRASH model included instrumental activity of daily living dependence, self-rated health status, Mini-Mental State score, and Mini-Nutritional Assessment (MNA) score.

Geriatric Assessment in the Oncology Setting: Specific Considerations

The GA can be applied in the oncology setting to identify potential areas of concern. Each domain within the GA focuses on a specific area, such as cognition or social support. These are areas not typically assessed by an oncologist during a routine evaluation, and yet there is growing evidence that geriatric domains have an impact on outcomes in older patients with cancer [18]. The various GA domains are discussed below, with specific considerations for the older oncology population.

Physical Function

Activities of daily living (ADLs) [19] and instrumental activities of daily living (IADLs) [20], as well as history of falls, are standard measures that are assessed within a GA. Objective physical performance is also measured using standardized tools such as the Short Physical Performance Battery (SPPB) [21] or Get Up and Go test [22]. As previously outlined, particular elements of physical function assessment, including fall history and IADL dependence, have been shown to be predictive of chemotherapy toxicity within the CARG and CRASH models [4••, 17••].

Comorbidity

Evaluation of competing comorbid conditions is an important consideration in assessing the older patient with cancer and developing a personalized cancer treatment plan [23]. Particular comorbid conditions may increase the likelihood of side effects of treatment. For example, patients with diabetes mellitus and peripheral neuropathy are at increased risk of developing accelerated neuropathy with certain types of chemotherapy such as taxanes [24]. Progressive neuropathy can further increase a patient’s risk of falls as well, and fall history should be evaluated when considering any chemotherapy agents that are known to cause neuropathy [25]. When evaluating a patient for adjuvant chemotherapy, estimated life expectancy should also be considered. Occasionally, because of competing serious comorbid conditions, patients will not live long enough to derive benefit from adjuvant chemotherapy, and treatment exposes them to potential side effects and complications [26].

Polypharmacy

A medication review should be conducted for all patients anticipated to begin cancer treatment. Particularly in the older patient, potential complications and side effects should be anticipated [27]. For example, in older patients on antihypertensive treatment, their nutrition and hydration may become compromised during chemotherapy treatment, which can predispose them to developing hypotension, placing them at increased risk of falls. Older patients with cancer receive numerous new medications (chemotherapy and supportive care) that may interact with ongoing medications [28].

Nutrition

In the general cancer population, pre-existing weight loss is an established risk factor for chemotherapy toxicity [29]. Poor nutritional status (≥10 % weight loss or low body mass index) has consistently been associated with early mortality in older patients with cancer [14, 30, 31]. Additionally, in the CRASH toxicity profile specific to older adults, MNA score has been shown to be a risk factor for non-hematologic toxicity [17••].

Cognition

Cancer treatment regimens are often complex, requiring frequent appointments and multi-step directions for home medication management. An understanding of baseline cognitive status is critical in determining a patient’s ability to comply with the proposed treatment plan. In the CRASH toxicity profile, cognitive impairment as defined by the Mini-Mental State score was shown to be predictive of non-hematologic toxicity [17••]. Furthermore, patients with more severe cognitive impairment may have difficulty identifying and reporting side effects from treatment. These patients may require a modification of their treatment regimen or increased supervision during course of treatment [3234]. While data are scarce with regard to the impact of chemotherapy on cognitive status in patients with pre-existing cognitive impairment, limited experiential data suggests that chemotherapy can accelerate cognitive impairment. Patients and families should be educated on the risks of delirium.

Social Support

Assessment of social support is also a critical factor in evaluating an older patient initiating cancer treatment. Most cancer treatments are administered on an outpatient basis, and patients often experience side effects that necessitate transportation assistance for treatment sessions. Moreover, the majority of side effects are experienced several hours to days after treatment, when patients are no longer in a medically supervised setting. In general, the most common side effect of chemotherapy is fatigue, and this can affect an older patient’s functional status and ability to perform IADLs and ADLs [35]. Occasionally, patients who live alone will require temporary alternative living arrangements during their treatment course for assistance in managing side effects and functional impairment. In appropriate situations, these options should be explored prior to initiation of therapy.

Psychological Status

Depression is common among older adults with cancer [9]. Untreated depression can exacerbate potential chemotherapy side effects such as fatigue and anorexia [36], and can affect quality of life [36]. Depression has also been shown to have an impact on overall survival in older adults with cancer [30].

Incorporating the Geriatric Assessment into Oncology Care

There are several models of care that incorporate GA into oncology practice. Most frequently, GA is performed in the outpatient setting in an attempt to minimize the impact of acute illness on functional and cognitive measures. Occasionally, however, inpatient evaluation may be necessary, depending upon the setting of diagnosis and treatment, and is more common for evaluation of patients with acute hematologic malignancies. GA is typically performed by a multidisciplinary team, and can be led by a geriatrician or geriatric oncologist.

The ELCAPA study evaluated the impact of GA on treatment decisions in a consultative clinic design [37•]. Patients were evaluated by a medical oncologist, and an initial treatment plan was developed. They were then referred for GA by a multidisciplinary team led by a geriatrician. The authors of the study found that the initial treatment plan was modified based upon GA results in 20.8 % of patients.

A study by Horgan et al. also explored the impact of GA in a consultative clinic format [38]. Patients aged 70 and older were evaluated by their primary oncologist and referred for geriatric assessment. Changes in initial treatment plan were recorded as the primary endpoint. The authors found that the majority of eligible patients were not referred for GA (71 %). Of the 30 patients who did undergo GA, the findings influenced treatment decisions in only six patients. The majority of these (83 %) occurred in patients where the initial treatment plan by the primary oncologist was not established prior to the consultation.

Potential drawbacks in the consultative clinic design include the fact that the final treatment plan is determined by the primary oncologists and may not reflect the recommendations of the geriatric consultant. Additionally, the consultative geriatric team may not continue to follow the patient during active treatment and may not be available for guidance if further geriatric-related issues develop. Given its consultative role within this model, however, the geriatric team is typically able to evaluate and influence care for a larger number of patients. Several cancer centers have adopted a consultative clinic design by “embedding” a geriatrician into their existing oncology clinic. The geriatrician functions as a member of the multidisciplinary team and is available to assist with geriatric-related issues as they arise. Some centers have utilized a geriatric-trained nurse practitioner or physician’s assistant in this role. Given the limited number of geriatricians, this is a feasible alternative in enhancing the role of geriatrics in the oncology setting.

Alternative models incorporate a geriatric oncologist as the primary provider for patients. Geriatric oncologists are dual-trained in hematology and/or medical oncology as well as geriatric medicine. In the primary provider model, a geriatric oncologist performs the initial assessment, develops the oncology treatment plan, and follows the patient throughout the course of treatment, managing any potential adverse side effects. The primary provider model is limited, however, due to the relatively few dual-trained geriatric oncologists available to assume this role.

The Role of the Screening Tool in Geriatric Oncology

When the geriatrician or geriatric oncologist operates as a consultant, the use of a screening tool may be helpful to identify patients for referral who are most likely to benefit from GA. With the increasing number of older patients with cancer and the limited availability of geriatric-trained providers, screening tools are an attractive option for selecting patients who are most apt to derive benefit from referral to a geriatrician or geriatric oncologist. A variety of screening tools exist, and to date there has been no “gold standard” identified with regard to the optimal tool. Numerous studies have evaluated potential screening tools in geriatric oncology, with the VES-13, Groningen Frailty Index (GFI), and G8 being the most commonly used. These tools are further described in Table 1. The majority of the studies evaluated the ability of the tool to predict deficits on the gold-standard geriatric assessment. It is important to note that this tool is not intended to replace geriatric evaluation and cannot provide a thorough assessment of an older individual’s health status. In addition, more information is needed with regard to screening tools and their relationship to outcomes, including chemotherapy toxicity, functional decline, and survival.

Table 1 Validated screening tools in geriatric oncology

Geriatric Assessment-Guided Interventions

In community-dwelling older adults, geriatricians utilize interventions to address impairments identified on GA. There is a moderate amount of data supporting the use of various interventions in this population. At present, there are no studies evaluating the impact of GA-guided interventions in older patients with cancer. Standard interventions are extrapolated from data derived from community-dwelling older patients (usually without cancer) to the oncology setting, with particular considerations. Table 2 outlines potential GA-guided interventions that can be utilized in the care of the older patient with cancer.

Table 2 Geriatric assessment-guided interventions for older patients with cancer

The University of Rochester Experience

The Specialized Oncology Care and Research in the Elderly (SOCARE) clinic at the University of Rochester was created for consultative geriatric oncology assessment for clinical and research purposes. In partnership with the University of Chicago, the clinic evaluates patents aged 65 and over with cancer who are referred for GA. The SOCARE clinic receives referrals from surgical, medical, and radiation oncologists who feel that GA would be beneficial in the development of a treatment plan for their patients. The multidisciplinary SOCARE team includes a geriatric oncologist, geriatric oncology fellow, nurse practitioner, geriatric-trained clinical nurse, physical therapist, occupational therapist, social worker, and clinic coordinator.

Prior to arriving for their appointment at the SOCARE clinic, all patients are asked to complete a self-administered questionnaire that includes ADL and IADL inventory, fall history, sarcopenia questionnaire, comorbidity screen, medication list, social support inventory, nutritional screen, geriatric depression screen (GDS), and worry scale. The assessment tool, which is 20 pages in length, is mailed to a new patient one week prior to the scheduled appointment. The majority of patients are independently able to complete the questionnaire, consistent with previously published evidence [49]. If assistance is required, the clinic coordinator is available to help patients complete their packet upon arrival for their appointment. The coordinator also completes objective physical performance assessment using SPPB and a cognitive screen using the Blessed Orientation-Memory-Concentration (BOMC) scale [50]. If there is evidence of weight loss or low BMI, MNA is also performed by the clinic coordinator. The team reviews the results of the GA and identifies areas of potential deficit. They also review cancer-specific details and proposed treatment options from the patient’s primary oncologist. Suggestions are made regarding treatment regimen preferences or potential modifications, and GA-guided interventions are developed based upon identified deficits. A clinical RN trained in geriatrics and oncology is available for patient and family education, with a particular focus on geriatric-specific issues that occur more commonly during cancer treatment (e.g., falls or delirium).

For patients with any identified physical functional impairments or history of falls, a physical therapist is available to provide education on fall prevention and training in ambulatory assist devices, development of an exercise program for strength, conditioning, and balance, and outpatient physical therapy referral. An occupational therapist (OT) is available to see patients to address upper-extremity strength and conditioning as well as ADL and IADL optimization, to counsel patients on energy conservation techniques, and to evaluate the need for outpatient occupational therapy referral. The OT has also received additional training on cognitive evaluation and is available to perform additional cognitive assessments (e.g., Montreal Cognitive Assessment [51]) when the preliminary cognitive screen is positive or there is a clinical concern of cognitive impairment. A social worker experienced in oncology and geriatrics meets with patients requiring social support interventions such as Meals on Wheels or home care agencies, personal emergency response system devices, and transportation assistance, and is also available to discuss alternative living arrangement options, health care proxy, and advance directives. A clinical pharmacist is available to review specific medication interactions and dosage modifications, and a clinical nutritionist is available to provide nutritional counseling and intervention recommendations for patients with impairment on nutritional screening.

The SOCARE clinic is a resource for clinicians and patients at a variety of time points during the course of treatment. Geriatric assessment can aid in clinical decision-making in various clinical situations, including:

  • Preoperative setting – evaluation prior to cancer surgery to assess surgical fitness and review the potential for postoperative functional impairment;

  • Adjuvant setting – quantify risks and benefits of adjuvant therapy, including consideration of additional comorbidities and geriatric syndromes with estimation of life expectancy;

  • Pretreatment assessment – evaluate and weigh the risks and benefits of multiple treatment options (e.g., sequential versus concurrent chemoradiotherapy, single-agent versus doublet chemotherapy regimens);

  • Survivorship – assist with management of geriatric-related conditions that may develop as a consequence of cancer-directed therapy.

Developing a Geriatric Oncology Clinic

Development of a geriatric oncology clinic can require resources and support from department administration. Unfortunately, at this time, there is no evidence to demonstrate that geriatric oncology clinics reduce the cost or utilization of health care or improve outcomes for patients. Studies evaluating these outcomes are underway. However, other rationales for the creation of geriatric oncology clinics include:

  1. 1)

    Identification of patients at increased risk of chemotherapy toxicity: Using the predictive models discussed above, geriatric oncology clinics can be helpful in the identification of patients at increased risk of complications and can potentially utilize these models to more appropriately select treatments for patients.

  2. 2)

    Reduction in time required by the medical oncologist to manage the complexity of the older patient: Geriatric oncology clinics foster the development of expertise in managing the complexities of older patients, including comorbidities, geriatric syndromes, complex social situations, physical impairments, and cognitive issues.

  3. 3)

    Fellow, resident, and medical student education: The Accreditation Council for Graduate Medical Education (ACGME) requires fellows in hematology/oncology to demonstrate an understanding of the interface between cancer and aging. A dedicated geriatric oncology clinic would support educational goals in this area.

  4. 4)

    Marketing value: Cancer centers with “expertise” in a specific area, such as geriatric oncology, provide marketing advantages in a community with multiple providers.

  5. 5)

    Patient-centered care: GA provides a complete health assessment as well an understanding of a patient’s values and social support network, which allows for a treatment approach tailored to each individual patient.

Conclusions

Geriatric assessment of the older patient with cancer can provide additional information about an individual’s overall health status in consideration of cancer treatment options. It has been demonstrated that the incorporation of GA into an oncology practice is feasible and is predictive of chemotherapy toxicity. Assessing an older patient’s physiologic age and functional status in conjunction with cancer-specific variables is helpful in the development of an overall treatment plan that is ideally suited to each patient. Although more research is needed to determine the effect of GA-guided interventions on outcomes of older patients with cancer, a geriatric oncology model of care can improve cancer treatment decision-making in the most complex settings for our older patients with cancer.