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    -  Irelli A
    -  Sirufo MM
    -  Scipioni T
    -  Aielli F
    -  Martella F
    -  Ginaldi L
    -  Pancotti A
    -  Martinis MD

 
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ORIGINAL ARTICLE
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The VES-13 and G-8 tools as predictors of toxicity associated with aromatase inhibitors in the adjuvant treatment of breast cancer in elderly patients: A single-center study


1 Medical Oncology Unit, Department of Oncology, AUSL 04 Teramo, Italy
2 Department of Life, Health and Environmental Sciences, University of L’Aquila, Italy; Allergy and Clinical Immunology Unit, Center for the Diagnosis and Treatment of Osteoporosis, AUSL 04 Teramo, Italy

Date of Submission25-Sep-2019
Date of Decision03-Nov-2019
Date of Acceptance21-May-2020
Date of Web Publication25-Jun-2021

Correspondence Address:
Massimo De Martinis,
Department of Life, Health and Environmental Sciences, University of L’Aquila, Italy; Allergy and Clinical Immunology Unit, Center for the Diagnosis and Treatment of Osteoporosis, AUSL 04 Teramo
Italy
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0019-509X.319470

 » Abstract 

Background: Adjuvant hormone treatment of postmenopausal breast cancer is mainly based on aromatase inhibitors. Adverse events associated with such class of drugs are particularly severe in elderly patients. Therefore, we investigated the possibility of ab initio predict which elderly patients could encounter toxicity.
Methods: In light of national and international oncological guidelines recommending the use of screening tests for multidimensional geriatric assessment in elderly patients aged ≥70 years and eligible for active cancer treatment, we assessed whether the Vulnerable Elder Survey (VES)-13 and the Geriatric (G)-8 could be predictors of toxicity associated with aromatase inhibitors. Seventy-seven consecutive patients aged ≥70 diagnosed with non-metastatic hormone-responsive breast cancer and therefore eligible for adjuvant hormone therapy with aromatase inhibitors, were screened with the VES-13 and the G-8, and underwent a six-monthly clinical and instrumental follow-up in our medical oncology unit, from September 2016 to March 2019 (30 months). Said patients were identified as vulnerable (VES-13 score ≥3 or G-8 score ≤14) and fit (VES-13 score <3 or G-8 score >14). The likelihood of experiencing toxicity is greater among vulnerable patients.
Results: The correlation between the VES-13 or the G-8 tools and the presence of adverse events is equal to 85.7% (p = 0.03). The VES-13 demonstrated 76.9% sensitivity, 90.2% specificity, 80.0% positive predictive value, 88.5% negative predictive value. The G-8 demonstrated 79.2% sensitivity, 88.7% specificity, 76% positive predictive value, 90.4% negative predictive value.
Conclusion: The VES-13 and the G-8 tools could be valuable predictors of the onset of toxicity associated with aromatase inhibitors in the adjuvant treatment of breast cancer in elderly patients aged ≥70.


Keywords: Aging, aromatase inhibitors, breast cancer, elderly, frailty, G-8 test, immunosenescence, toxicity, VES-13 test
Key Message: The VES-13 and the G8 tools could be valuable predictors of toxicity associated with aromatase inhibitors in the adjuvant treatment of breast cancer in elderly patients aged ≥70.



How to cite this URL:
Irelli A, Sirufo MM, Scipioni T, Aielli F, Martella F, Ginaldi L, Pancotti A, Martinis MD. The VES-13 and G-8 tools as predictors of toxicity associated with aromatase inhibitors in the adjuvant treatment of breast cancer in elderly patients: A single-center study. Indian J Cancer [Epub ahead of print] [cited 2021 Jul 27]. Available from: https://www.indianjcancer.com/preprintarticle.asp?id=319470



 » Introduction Top


Hormone receptor-positive breast cancer, i.e., in the presence of estrogen receptor (ER)-positive (≥1%) or progesterone receptor (PgR)-positive (≥1%), must be treated with hormone therapy with or without chemotherapy. Postmenopausal women should be treated with aromatase inhibitors for 5 years, or sequential tamoxifen for 2–3 years followed by an aromatase inhibitor for 2–3 years.[1],[2] The Early Breast Cancer Trialists' Collaborative Group (EBCTCG) meta-analysis showed that 5 years of upfront aromatase inhibitors reduce breast cancer mortality to 10 years—15% when compared to tamoxifen. Postmenopausal women who have completed 5 years of adjuvant tamoxifen treatment, should be treated with an aromatase inhibitor for an additional 5 years, following an assessment of benefit-to-damage ratio (in terms of toxicity) and risk for relapse.[3]

It is reported that an increase in the risk of cardiovascular adverse events such as ischemic heart disease (inconclusive data), hypercholesterolemia, hypertension, alterations in glucose and lipid metabolism as well as musculoskeletal toxicity (bone mineral density (BMD) reduction, increased risk of skeletal fractures, arthromyalgia),[4],[5],[6] yet a minor incidence of thromboembolic and endometrial tumor phenomena in aromatase inhibitor versus tamoxifen treatment. Cerebrovascular events seemingly showed no variations. Musculoskeletal adverse events are clinically important as they commonly cause hormone therapy interruption.

The assessment of the extended aromatase inhibitor treatment (over 5 years), resulted in a greater likelihood of toxicity.[7]

The management of cancer in the elderly is a major public health concern in most countries and a Comprehensive Geriatric Assessment (CGA) would be beneficial in this frail population often with comorbidities to ensure better results.[8],[9],[10],[11]


 » Materials and Methods Top


Study design

This prospective observational study aims to assess whether the Vulnerable Elder Survey (VES)-13 [Figure 1] and the Geriatric (G)-8 [Figure 2] screening tests can be valuable predictors of toxicity associated with aromatase inhibitors in the adjuvant treatment of breast cancer in elderly patients aged ≥ 70. This was a 30-month study, from the first patient being recruited to the cut-off date. Each enrolled patient was followed for a 6-month follow-up. The toxicity assessment was performed every 3 months.
Figure 1: The Vulnerable Elder Survey (VES)-13 screening tool[33]

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Figure 2: The Geriatric (G) 8 screening tool[33]


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Patient eligibility

The eligiblity criteria of the study included: women aged ≥70, the histopathological diagnosis of breast cancer with positive hormone receptors, clinical-instrumental baseline tests resulting negative for metastasis. Previous chemotherapy treatment was allowed. All patients were subjected to the VES-13 and the G-8 screening tools, thus divided into vulnerable patients (VES-13 ≥3 or G-8 ≤14) and fit patients (VES-13 <3 or G-8 >14). All patients underwent a six-monthly clinical and instrumental follow-up along with questioning about the symptoms presented during the oncological check-ups, to detect any adverse events associated with aromatase inhibitors.

Ethics

The study was approved by our Internal Review Board and conducted in accordance with the 1975 Helsinki Declaration and its subsequent amendments. Written informed consent was obtained from all individual participants included in the study.

Assessment of safety and statistical analysis

Adverse events were assessed every 6 months since the start of hormone therapy and were encoded through the use of the Common Terminology Criteria for Adverse Events (CTCAE) V4.03. Statistical analysis was performed through the use of Microsoft Excel 2013 on Windows 7 Professional (2009 version). The χ2 test was used to compare the identified patient subgroups. P value ≤ 0.005 was considered statistically significant.


 » Results Top


Patients' features

This is a prospective observational study concerning 77 consecutive patients diagnosed with breast cancer and treated with aromatase inhibitors in the adjuvant setting, in our Medical Oncology Unit, from September 2016 to March 2019 (30 months). The patients were screened through the VES-13 test and divided into vulnerable patients (VES-13 ≥3 or G-8 ≤14) and fit patients (VES-13 <3 or G-8 >14) [Table 1] and [Table 2]. The median age of all patients was 76 years (ranging from 70 to 90 years old), 76 years for the vulnerable group (70–90 years old), 76 years for the fit group (70–84 years old). A total of 29 (37.7%) patients were previously treated with chemotherapy, 4 (15.4% for the VES-13 and 16.7% for the G-8 test) in the vulnerable group, 25 (49.0% for the VES-13 and 47.2% for the G-8 test) in the fit group.
Table 1: Clinical characteristcs of patients


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Table 2: Clinical characteristics of patients


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Safety

By analyzing toxicities, we found 25 (32.5%) out of 77 patients reporting all levels of toxicity, i.e., 20 (76.9%) vulnerable patients out of 26 and 5 (9.8%) fit patients out of 51 (p < 0.001) among patients undergoing the VES-13 test [Table 1] and 19 (79.2%) vulnerable patients out of 24 and 6 (11.3%) fit patients out of 53 (p < 0.001) among patients undergoing the G-8 test [Table 2].

Adverse events were: arthromyalgia [G3 in 2 (2.6%) patients], arthromyalgia [G1 in 15 (19.5%) patients], arthromyalgia [G2 in 5 (6.5%) patients], thromboembolic event [G2 in 1 (1.3%) patients], depression [G1 in 2 (2.6%) patients].

Among patients undergoing the VES-13 test, vulnerable patients were more likely to experience toxicity: arthromyalgia [G3 in 2 (7.7%) patients], arthromyalgia [G2 in 3 (11.5%) patients], arthromyalgia [G1 in 12 (46.1%) patients], thromboembolic event [G2 in 1 (3.8%) patients], depression [G1 in 2 (7.7%) patients]; whereas adverse events among fit patients were: arthromyalgia [G2 in 2 (3.9%) patients], arthromyalgia [G1 in 3 (5.9%) patients] [Table 3].
Table 3: Toxicity (all grades) in vulnerable patients, fit patients, and all patients


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Among patients undergoing the VES-13 test, vulnerable patients were more likely to experience toxicity: arthromyalgia [G3 in 2 (8.3% patients], arthromyalgia [G2 in 3 (12.5%) patients], thromboembolic event [G1 in 11 (45.8%) patients], depression [G1 in 2 (8.3%) patients]; whereas adverse events among fit patients were: arthromyalgia [G2 in 2 (3.8%) patients], arthromyalgia [G1 in 4 (7.5%) patients] [Table 4].
Table 4: Toxicity (all grades) in vulnerable patients, fit patients, and all patients


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Efficacy

The closeness of agreement between the VES-13/G-8 tools and the presence or absence of adverse events was 85.7% (P = 0.03). The VES-13 test showed 76.9% sensitivity, 90.2%, specificity, 80.0% positive predictive value, 88.5% negative predictive value. The G-8 test showed 79.2% sensitivity, 88.7%, specificity, 76.0% positive predictive value, 90.4% negative predictive value [Table 5].
Table 5: Diagnostic accuracy of VES - 13 and G-8 tools as predictor of toxicity associated with aromatase inhibitors in the adjuvant treatment of breast cancer in elderly patients


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 » Discussion Top


Having the highest incidence, breast cancer is also the leading cause of cancer-related death among western women. Breast tumors represent the most frequently diagnosed form of cancer among women aged over 70 years (about 22%).[12] Cancer risk increases with age. With longer life expectancy, the understanding of geriatric parameters becomes increasingly important among oncologists when setting correct/adequate active oncological treatments. Physiologically in the elderly, we observe the progressive decline in functional reserve of multiple organs and systems with different levels of susceptibility in the aging population.[13] More susceptible subjects have a higher risk of negative health outcomes and probability to develop treatment complications.[14] Tolerance to anticancer treatment can be reduced due to aging-related changes so that in older cancer patients the overall risk-benefit ratio for treatment can shift and a risk-adapted therapy approach become indispensable with the early recognition of susceptible people.

Cancer and its therapy are significant stressors that may increase vulnerability to develop dependency and/or mortality and this clinical state is defined “frailty”. So, frailty is a relevant issue in oncology as geriatric patients are at risk of overtreatment. Frailty is a state that can rapidly change over time worsening or improving. It may be psychological, physical or both, often asymptomatic or subtle, where people may be autonomous but at high-risk of developing a disability. Since 2013 six major U.S. and European scientific societies agreed on the necessity of subjecting all persons aged ≥70 for frailty to better manage people with physical frailty and these appear to be particularly fitting in oncology although still quite neglected in practice. Cancer patients, among others, are more likely to be frail and to have more adverse outcomes and simple screening tests are available to judge the appropriateness of some treatments to improve overall outcomes. Older adults with cancer are rapidly growing, clinical practice has time constraints and needs tools to rapidly assess older's fitness for treatment decisions.[15] Clinical practice worldwide must successfully combat frailty implementing its screening and management to better deliver the most adequate and personalized cancer treatments. Despite ongoing efforts to improve the quality of care of older cancer patients, geriatric oncology still has a long way to go to better understand cancer treatments' effectiveness, safety, and tolerability to really impact an elderly centered outcome.[16],[17] The International Society of Geriatric Oncology (SIOG) has set up a working group with the aim to outline a CGA in cancer patients aged ≥65–70 years and eligible for active cancer treatments.[18] Being used by geriatricians and oncologists, the CGA analyzes the domains related to functional status, cognitive status, mood, nutritional status, comorbidity, and polypharmacy therapies—it allows planning and coordination of geriatric interventions, leading to adapted cancer treatment.[19] The CGA improves the management of the elderly patient population resulting in improved functional status and survival rate, and it is therefore economically advantageous as it leads to a drop in the rate of hospitalization.[18] However, The CGA is time-consuming, thus efforts have been made to find suitable screening tests able to provide elderly patients with a multidimensional geriatric assessment. In this regard, SIOG guidelines recommend the use of screening tests such as G-8 and the VES-13.

Among others, the VES-13 is a self-reported function-based scoring system that considers age, self-rated health, physical performance, and functional status to measure frailty. It is a useful and proven tool to screen the risk of health deterioration in already vulnerable elderly subjects. It has been indicated that a VES-13 score ≥3 identifies frail cancer patients.[20],[21] The VES-13 is a scoring system based on a 13-item questionnaire that can be filled out by the patient. The test includes information such as age groups (65/70–74, 75–84, ≥85), perceived health status (excellent, very good, good, poor, bad), difficulty level in performing six daily activities (kneeling, crouching, bending over, lifting and carrying a 4.5 kg (9.92 lb) object, extending the arm above shoulders, writing, holding up a small object, walking 400 meters (1300 feet), heavy-duty tasks such as washing floor/windows) and difficulty level in performing five instrumental daily activities (shopping, handling cash, walking around the room, doing housework, bathing, and showering). The maximum score is 10, with a cut-off score of 3 points, beyond which the risk of vulnerability is high. The VES-13 can be predictive of impairment in functional status which was analyzed through activities of daily living (ADLs) and instrumental activities of daily living (IADLs) assessment forms,[22] as well as the cumulative illness rating scale (CIRS) and the short portable mental status questionnaire (SPMSQ).[23] Therefore, the VES-13 score reveals the risk of health deterioration in the elderly population and its highest score reflects a higher risk in a short follow-up period.[24] The role of the VES-13 test in the management of elderly cancer patients is yet to be determined, however, data show that the VES-13 is heavily studied in geriatric oncology. The VES-13 may, in fact, allow the identification of elderly patients being at risk of toxicity related to cancer treatment. This new potential role has been described in a few previous studies.[25],[26],[27] The study by Luciani et al. is a pooled analysis of four published clinical trials regarding the VES-13 as a means to diagnose vulnerability with the aim of assessing its accuracy in predicting the risk of grade 3/4 toxicity in elderly patients who receive chemotherapy.[28] Whether it is hematological or not, grade 3-4 toxicity was prevalent in vulnerable subjects.[29]

Self-completion of the VES-13 test has often been problematic and about 40% of patients unable to complete the test themselves are reported in the literature. In patients with various cancers, VES-13 was predictive of the occurrence of severe toxicity from chemotherapy (p = 0.015).

The G-8 is a screening tool of eight items concerning food intake, weight loss, movement, neuropsychological problems (dementia or depression), body mass index, taking more than three types of drugs, assessing one's health, age (>85, 80–85, <80 years old). The total score ranges from 0 to 17. A score ≤14 is considered abnormal. In various cancers, G-8 was predictive of chemotherapy-related toxicity (p = 0.025).

Two studies that looked at both VES-13 and G-8 suggested that a combination of both tools is a more sensitive screening tool. Pottel et al. demonstrated that VES13 + 17-G-8 ≥5 has a sensitivity of 91.4% and a specificity of 93.8%.[30] The combination of both instruments was significantly better than the G-8 or VES-13 alone (p = 0.024 and P = 0.0237). Maximum sensitivity was observed with the G-8 test (>80%). The G-8 has shown good sensitivity. The results are more heterogeneous for the VES-13 test. Soubeyran et al. found that an abnormal G-8 or VES13 tools demonstrated 86.6% sensitivity and 53.2% specificity for detecting patients unsuitable for geriatric assessment.[31]

The diagnostic accuracy of G-8 and VES-13 tools was assessed in a prospective cohort study with 1674 cancer patients and evaluable before treatment, in 23 healthcare facilities. Outcome measures included sensitivity and specificity. The mean age of the patient was 78.2 years (70–98) with the majority (69.8%) being women, various types of cancer including 53.9% of the breast. G-8 appeared more sensitive (76.5% versus 68.7%, P = 0.0046) while VES-13 was more specific (74.3% versus 64.4%, P < 0.0001).[31]

In this prospective observational study, we assessed the role of the VES-13 test and the G-8 test as possible predictors of toxicity associated with aromatase inhibitors being used in the precautionary treatment of elderly patients with non-metastatic breast cancer and removed invasive carcinoma with positive hormone receptors.

Among vulnerable patients, we identified 76.9% and 73.2% of patients with aromatase inhibitor toxicity, with the VES-13 test and the G-8 test, respectively. Among fit patients, we identified 9.8% and 11.3% of patients with aromatase inhibitor toxicity, with the VES-13 test and the G-8 test respectively.

These two tools use items that require a short compilation time, maximum 5 minutes each, and therefore in clinical practice, they are easily administered to the patients we see in the clinic. In the VES-13 screening test, only such questions are inserted, which try to probe the patient's perception of their health in relation to their age, bringing to light the difficulties that occur in carrying out common actions of daily life that connote the state of independence. In the G-8 screening test, however, in addition to asking the patient to perceive their health in relation to their age, great attention is paid to the aspect of nutrition and comorbidities by requesting notification of the number of drugs they are taking. (> or <3). When administering a test to a patient, the patient is called to read, understand, and elaborate the writing; this inevitably also clashes with the patient's cultural level. In our clinical practice, patients asked for help to understand and therefore answer questions more in the VES-13 test than G-8.

Dottorini et al. recently published a paper in which the G-8 test was used to predict side effects during adjuvant treatment with aromatase inhibitors in women aged ≥65 and affected by breast cancer. Through the test, patients aged ≥65 were identified as fit (G-8 score >14) and vulnerable (G-8 score ≤14) - 30 (60%) and 20 (40%) patients, respectively. The closeness of agreement between the G-8 score and the occurrence and nonoccurrence of adverse events was statistically significant (41/50 patients, 82%, P = 0.0002), the sensitivity of the G-8 test was 78%, 81% specificity, 70% positive predictive value, and 87% negative predictive value. Arthromyalgia resulted in being the most frequent adverse event.[32]

In our study, through the VES-13 test, patients aged ≥70 were divided into 26 (33.8%) vulnerable patients (VES-13 ≥3) and 51 (66.2%) fit patients (VES-13 <3). The closeness of agreement between VES-13 and the presence or absence of adverse events was 85.7% (66/77 patients, P = 0.03). The VES-13 test showed 76.9% sensitivity, 80.2% specificity, 80.0%, positive predictive value, 88.5% negative predictive value. Furthermore, in our study, through the G-8 test, patients aged ≥70 were divided into 24 (31.2%) vulnerable patients (G-8 ≤14) and 53 (68.8%) fit patients (G-8 >14). The closeness of agreement between G-8 and the presence or absence of adverse events was 85.7% (66/77 patients, P = 0.03). The G-8 test showed 79.2% sensitivity, 88.7% specificity, 76.0%, positive predictive value, 90.4% negative predictive value. Hence, in our experience, the VES-13 test was more sensitive and less specific than the G-8 test, similarly to the literature data [Table 6].[33]
Table 6: Comparison of the diagnostic accuracy of the screening tools between our study and Dottorini et al. study[32] in prediction of toxicity associated with aromatase inhibitors in the adjuvant treatment of breast cancer in elderly patients


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In this study as well, arthromyalgia resulted in being the most frequent adverse event.

By comparing the two aforementioned studies, it is possible to outline the relationship between the G-8 and VES-13 screening tests as helpful tools for clinical oncologists when predicting the tolerability of aromatase inhibitors among elderly patients in the adjuvant setting. The management of aromatase inhibitor toxicity has not been reported in this study as it did not affect the study objectives. However, this study presents significant limitations as it is a prospective observational analysis conducted in a single center and concerning a small sample of patients. Moreover, this study is single-arm and is conducted on a cohort of elderly patients in the absence of the control group of young patients. Therefore, regarding the use of the VES-13 or the G-8 tests in clinical practice, no definitive conclusion can be reached. This study demonstrates that the use of the VES-13 and the G-8 screening tools could be predictive of toxicity associated with aromatase inhibitors in the adjuvant setting of breast cancer in elderly patients aged ≥ 70 years. According to this study, it is necessary to conduct further research with a larger, multicentric, patient population, to demonstrate the unequivocal necessity to use screening tests such as the VES-13 in the selection of active treatment of elderly patients.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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