Introduction
Mexico is a middle-income country, with a population of almost 130 million, is the second-largest economy in Latin America (The World Bank 2023). The country is undergoing an intense process of change that involves multiple transitions in the economic, social, political, urban, epidemiological, and demographic spheres (Salinas-Rodríguez et al. Reference Salinas-Rodríguez, Manrique-Espinoza and Heredia-Pi2019); (The World Bank 2023).
The total number of older adults, aged 60 years and older, will triplicate, from 6.3% in 2010 to almost 23% by 2050 (Angel et al. Reference Angel, Vega and López-Ortega2017). Aging has led to an increased incidence of cancer cases worldwide. In fact, it is expected that by 2035, aging will represent 58% of the global burden of cancer incidence (Pilleron et al. Reference Pilleron, Sarfati and Janssen-Heijnen2019) and it is estimated that by 2050 6.9 million new cancer cases will be diagnosed in the elderly of >80 years worldwide (20.5% of all cancer cases) (Centro de Investigación en Evaluación y Encuestas. Informe de Resultados de la Encuesta Nacional de Salud y Nutrición – Reference Shamah-Levy, Romero-Martínez and Barrientos-Gutiérrez2022 n.d.; Yancik Reference Yancik2005).
Many factors, including social determinants of health, geriatric syndromes, organ function, transportation, ageism, access, and assessment, play a role in creating barriers to equitable care for older adults with cancer; in consequence, late cancer diagnosis, suboptimal treatment, poor symptom management, worsen survival, and quality of life (Brant Reference Brant2018; Centro de Investigación en Evaluación y Encuestas. Informe de Resultados de la Encuesta Nacional de Salud y Nutrición – Reference Shamah-Levy, Romero-Martínez and Barrientos-Gutiérrez2022 n.d.; Parajuli et al. Reference Parajuli, Tark and Jao2020; Salinas-Rodríguez et al. Reference Salinas-Rodríguez, Manrique-Espinoza and Heredia-Pi2019; Yancik Reference Yancik2005).
Older adults with cancer have complex needs, those related comorbid conditions, fragility, medication, that are specific of geriatric; and palliative care needs (cancer-related symptoms, psychological and spiritual problems (Brant Reference Brant2018; Brighi et al. Reference Brighi, Balducci and Biasco2014)) for older adults with cancer, palliative care consultation alone may not fully address all their concurrent medical and psychosocial comorbidities, and geriatricians may not address patients palliative care needs (Brighi et al. Reference Brighi, Balducci and Biasco2014; Nipp et al. Reference Nipp, Temel and Fuh2020).
The development of services for the older patient with cancer has been addressed at different levels, multiple organizations including the American Society of Clinical Oncology, (Mohile et al. Reference Mohile, Dale and Somerfield2018) the International Society of Geriatric Oncology, (Extermann et al. Reference Extermann, Aapro and Bernabei2005; Klepin et al. Reference Klepin, Rao and Pardee2014), and the National Comprehensive Cancer Network (Denkinger et al. Reference Denkinger, Knol and Cherubini2023; Dotan et al. Reference Dotan, Walter and Browner2021), all recommend the inclusion of geriatric principles into cancer care for older adults. There is no specific model, and adoption depends on local interest, funding, and available staff. Several models of care have been described. These models include a consultative geriatric assessment, a geriatrician in an oncology clinic, and primary management by a dual-trained geriatric oncologist (Berman et al. Reference Berman, Davies and Cooksley2020; Brant Reference Brant2018; Brighi et al. Reference Brighi, Balducci and Biasco2014; Festen et al. Reference Festen, De Graeff and Rostoft2023; Gomez-Moreno et al. Reference Gomez-Moreno, Verduzco-Aguirre and Soto-perez-de-celis2020; Hui and Bruera Reference Hui and Bruera2020; Seghers et al. Reference Seghers, Alibhai and Battisti2023; Soo et al. Reference Soo, Yin and Crowe2023; Soto Perez De Celis et al. Reference Soto Perez De Celis, Navarrete Reyes and Vazquez Valdez2016; Verduzco‐Aguirre et al. Reference Verduzco‐Aguirre, Navarrete‐Reyes and Chavarri‐Guerra2019; Voumard et al. Reference Voumard, Rubli Truchard and Benaroyo2018; Williams et al. Reference Williams, Hopkins and Klepin2023). In the Mexican public healthcare sector, for elderly cancer the first geriatric oncology clinic was created at the Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán in 2015, as a consultative model, where recommendations are given to the primary treating oncologist or hematologist (Gomez-Moreno et al. Reference Gomez-Moreno, Verduzco-Aguirre and Soto-perez-de-celis2020; Soto Perez De Celis et al. Reference Soto Perez De Celis, Navarrete Reyes and Vazquez Valdez2016; Verduzco‐Aguirre et al. Reference Verduzco‐Aguirre, Navarrete‐Reyes and Chavarri‐Guerra2019).
At the Instituto Nacional de Cancerología (INCan), an European Society for Medical Oncology (ESMO), Designated Centre of Integrated Oncology & Palliative Care, we developed a comprehensive transdisciplinary approach for the care of older adults with advanced cancer, which included integrative training to blend the disciplines of geriatrics and palliative care (Allende-Pérez et al. Reference Allende-Pérez, Verástegui-Avilés and Mohar-Betancourt2016; ESMO 2022).
The geriatric palliative care clinic (GPCC, Table 1) like the geriatric palliative care emphasizes the patient-centered assessment that included physical and psychological symptom concerns, comorbid conditions and polypharmacy, cognitive issues, availability of social supports, functional status assessment, fragility, cancer-related issues, and palliative care needs (Ocampo-Chaparro et al. Reference Ocampo-Chaparro, Reyes-Ortiz and Etayo-Ruiz2021; Santivasi et al. Reference Santivasi, Partain and Whitford2020; SECPAL. Sociedad española de Cuidados paliativos 2014; Tinitana Soto et al. Reference Tinitana Soto, Herrera Sarango and Cárdenas Estrella2023; Voumard et al. Reference Voumard, Rubli Truchard and Benaroyo2018).
Table 1. Summary of relevant terminology in geriatric palliative care
Palliative care model in the elderly with cancer
The number of older patients with cancer has increased in Mexico, our model started in 2016 with approximately 1500 first consultations in people aged 60 years and older. Later due to multiple needs involving the care of these patients the work continued but this time with people aged 70 and over, thus, after an extensive review of the literature describing healthcare models for older patients with cancer, a comprehensive clinical care model, including the 4 components of a holistic approach (physical, psychological, spiritual, and social) was established at our center. Geriatric palliative care specialist (GPCS) is an essential piece and plays a fundamental role within this integrated model by being part of the palliative care team and by functioning as a liaison, maintaining close and direct communication with the oncology team, and supporting the management of symptoms, comorbidities, geriatric syndromes, as well as performing comprehensive geriatric assessment and helping in decision-making (Figure 1).
Figure 1. Comprehensive care clinic model geriatric palliative.
The objective of this article is to describe the profile of the population attended to by the palliative geriatrics clinic and to evaluate the symptomatic control derived from the care provided.
Methods
Patients and data
During 2017–2019, 423 patients aged ≥70 years were referred to the palliative care service.
The profile of these patients is described. Of them, 100 patients were selected with simple random sampling. With ages ≥70, both genders and any cancer diagnosis. Demographic and clinical characteristics, including geriatric syndromes, as well as the Karnofsky Performance Status and Edmonton Symptom Assessment System-Revised (ESAS-r) (Carvajal et al. Reference Carvajal, Hribernik and Duarte2013) from the initial and the subsequent (1 month) consultations, were obtained from the institutional electronic medical records.
For study analysis purposes, the sample was divided into 2 groups. Group A with patients 70 years of age or older without cancer treatment and group B with patients 70 years of age or older with active cancer treatment (support in supportive care). Both groups received support from the team geriatric palliative care for the symptomatic management (Figure 2).
Figure 2. Palliative care model for older adults with cancer at the National Cancer Institute in Mexico.
To assess the complexity of the patients, the Diagnostic Instrument for the complexity of cases in Palliative Care (IDC-Pal instrument) was used, which considers elements related to functionality, symptom control, cognitive status of patients, socioeconomic level, family dynamics, communication and information presented between those involved in each case, ethical considerations, therapeutic intervention needs, and the relationship between the patient and the healthcare team (Roselló et al Reference Roselló, Fernández-López and Sanz-Amoresn.d.; Salvador Comino et al. Reference Salvador Comino, Garrido Torres and Perea Cejudo2017).
This study was approved by the Institutional Review Board (Ethics in Research and Research Committees [REF/INCAN/CI/0622/2019]).
Statistical analysis
Descriptive statistics included the median and interquartile ranges (IQRs) for numerical variables and frequencies and percentages for categorical variables. Comparisons were performed according to the type of variable, chi-square/Fisher’s exact test and Wilcoxon rank test for categorical and numerical variables, respectively. A p-value <0.05 was considered statistically significant. All the analyses were performed using the Stata 12 software (StataCorp 2011 Stata Statistical Software: Release 12. College Station, TX: StataCorp LP).
Results
Referral to palliative care
During this period 423 patients aged ≥70 years were referred to the palliative care service. Patients had a median age of 83 years, females (60%), 45% married, 53.7% living in poverty; 72% had <6 years of formal education. The most common cancer type was hematological (18%), head and neck cancer (15%), gynecological cancer (12%), gastrointestinal (11%), urological cancer (9.0%), and breast cancer (9.0%)
In the subgroup of 100 patients, the median age of the patients included was 83.5 years; mostly females; and their educational background was mainly elementary school or none (76%). The main caregiver was the patient’s son or daughter (73%), followed by the partner or spouse (14%); 82% had no formal employment. The median monthly income was 202.67USD (IQR: 108.49–369.58 USD). Table 2 shows the overall demographic and clinical characteristics of all the patients. Patients were grouped by type of management: 47% within the supportive care group and 53% with palliative care only. The 5 most frequent cancer diagnosis were lymphoma, prostate, lung, breast, and ovarian, which accounted for a total of 60%; 58% had metastatic disease, 84% presented at least 1 comorbidity, and from the latter, 7% had between 5 and 9 comorbidities.
Table 2. Demographic and clinical characteristics of elderly cancer patients of the geriatric palliative care clinic model
a IQR = interquartile range.
* statistically significant.
Fifty-three percent of the patients had 2 or more comorbidities and 25% of the frail patients presented at least 5 comorbidities. A Karnofsky score of 60 or less was observed in 59% of the patients with palliative care only, representing a high percentage.
Regarding the geriatric assessments, 66% had unsteady gait, 32% suffered recurrent falls and, 21% were immobilized. Half of the patients showed dependence, either partially or totally, in daily life activities (DLAs), which was more frequent among those undergoing palliative care. Frailty occurred in 78% of the patients, being more frequent in the group with only palliative management. Polypharmacy was present in 87% (Table 3).
Table 3. Geriatric syndromes in older cancer patients of the geriatric palliative care clinic model
a DLAs = daily life activities.
* statistically significant.
Figure 3 shows the ratings and comparisons of the intensity of the symptoms between the initial and subsequent appointment assessments among all the patients of this study (p < 0.05).
Figure 3. Changes in symptom intensity according to the initial and subsequent consultation measurements (only symptoms with statistically significant differences between both measurements were plotted).
The median overall survival of the total population was 508 days (IQR: 223–1978 days). According to the type of management, the median survival in patients undergoing palliative and supportive care was 252 (IQR: 87–610 days) and 1059 days (IQR: 444-not reached), respectively. A statistical significance was observed (p = 0.00001).
Complexity
Forty-six percent were classified as “highly complex” and “complex” in 32% of cases. Of the highly complex items, the most frequent was “clinical situations secondary to tumor progression that is difficult to manage.” In the category of clinical situation, 4 items stand out with significant frequencies in “complex” patients in descending order: “severe cognitive disorder,” “difficult clinical management due to repeated therapeutic noncompliance,” “severe constitutional syndrome,” and “existence of comorbidity that is difficult to control” (Figure 4 and Table 4).
Figure 4. Complexity in palliative care (frequency 5% or higher).
Table 4. Diagnostic instrument of complexity in palliative care
Discussion
There are plenty of opportunities within the care of older cancer patients. Thus, it is reasonable to consider them a special subgroup that requires individualized interventions. Despite the extensive literature on the overall integration of palliative care, only few studies have described specific plans and their impact on the elderly patients with cancer (Berman et al. Reference Berman, Davies and Cooksley2020) and the role of the GPCS. This study reports the results of an integrative care clinic model established since 2017, in which the GPCS was included as part of the transdisciplinary care of these patients and their families. Our model was designed to address the current patients’ and the institutional unmet needs resulting from the increased population of older cancer patients requiring specialized geriatric care.
More importantly, taking into account that there are few geriatric oncologists in our country that meet the required needs, our model seeks to solve as many requirements as possible in order to potentially reduce disparities within the care of these patients. This being a pilot educational model to meet the country needs (Allende-Pérez et al. Reference Allende-Pérez, Verástegui-Avilés and Mohar-Betancourt2016; ESMO 2022). Accordingly, the main objective of the implemented care clinic model approach was to assist the oncology team in the decision-making process, detection of frail patients, symptoms control, and management of comorbidities and associated geriatric syndromes, in patients requiring both supportive and palliative care, by providing a more integrated perspective along with the oncology team.
This study describes the profile of patients seen in a period of 2 years by the geriatric clinic, accompanied by an analysis of the characteristics of a small group of elderly cancer patients seen at the recently established GPCC. Among them, we observed a profile of vulnerability and complexity from a clinical standpoint. A large proportion were women, with none or very basic educational attainment, low socioeconomic status, multiple comorbidities, polypharmacy, with cognitive alterations and repetitive therapeutic noncompliance, which was consistent with data reported in previous studies (Pal and Manning Reference Pal and Manning2014). The most frequent cancer diagnoses (lymphoma, prostate, lung, breast, and ovarian) referred to palliative care were those already reported to be the most common among the Mexican population (Gomez-Moreno et al. Reference Gomez-Moreno, Verduzco-Aguirre and Soto-perez-de-celis2020). Conversely, most patients had advanced cancer and many required assistance in at least 1 DLA. Performance status was relatively low, especially among those patients undergoing palliative care, a potential explanation refers to the dates when the model was established, as many of those patients were exclusively followed-up by the oncology team and only a minority had already been referred to palliative care from the beginning, which can limit care in these patients. That is why the importance of earlier diagnoses and referrals, preferably made immediately after the first institutional admission and evaluation of the patient with a comprehensive geriatric model that contemplates early referral, emphasizing care for fragile patients.
Elderly patients represent a significant proportion of the cancer patients and about 80% of the annual cancer-related deaths. Frailty is of particular interest in cancer (Goede Reference Goede2023; Pal and Manning Reference Pal and Manning2014) as it has been associated with adverse health outcomes in this context (Ethun et al. Reference Ethun, Bilen and Jani2017; Ho et al. Reference Ho, Tang and Chen2021; Mima and Baba Reference Mima and Baba2023). In our study, 78% of the patients were frail, this could be explained by the fact that the highest frequency of frail patients is found in the palliative care group, which was characterized by late referral and greater functional dependence. Similar results were reported in a systematic review; the prevalence of overall frailty in cancer patients was 42% (range: 6%–86%) (Handforth et al. Reference Handforth, Clegg and Young2015).
In our study, we identified that frail patients had a higher number of comorbidities, more falls, and a low Karnofsky score. As we also observed statistical significance when comparing these results with those from the subgroup of patients without frailty, findings that may be relevant due to their association with adverse outcomes. Therefore, early detection and measurement of frailty by the oncology team is important to start working in conjunction with the palliative care service, which in turn would facilitate the involvement of patients and their families in the decision-making process about management and prognosis plans.
The reference of frail patients should be complemented with a comprehensive geriatric assessment in these patients, since in addition to helping us detect frailty, it can help determine the life expectancy of these patients, as well as estimate the functional status reserve and tolerance to chemotherapy, as well as contributing to symptomatic treatment and geriatric syndromes, which is very important for management and decision-making in older adult patients with cancer.
Hence, symptom control is one of the main principles and goals of palliative care and so, of our model. It has been shown in certain groups of patients that palliative care interventions successfully controlled symptoms and improved the quality of life (Allende-Pérez et al. Reference Allende-Pérez, Sánchez-Dávila and Peña-Nieves2021; Gaertner et al. Reference Gaertner, Siemens and Meerpohl2017; Holmenlund et al. Reference Holmenlund, Sjøgren and Nordly2017; Temel et al. Reference Temel, Greer and Muzikansky2010). In our study, results were statistically significant (p < 0.05) after the intervention of the GPCS. Improvements were observed within the patients’ symptoms and overall well-being. These results can be associated with the intervention of the GPCS, since we believe that its preparation both in theoretical knowledge of geriatrics, as well as its expertise in palliative care and symptom management can contribute to an intervention with a greater impact on symptom control. Although only 2 measurements were performed (during the initial and 1-month appointments), we acknowledge that follow-up will be important for future research. Furthermore, another key element will include the medium and long-term follow-up in the control of symptoms, as well as measuring the quality of life before and after interventions, in addition, the inclusion of a reference group that would allow direct comparisons would be relevant when applicable.
We have previously reported that the median survival for palliative cancer patients in our clinic was 3.1 months (Allende-Perez et al. Reference Allende-Perez, Peña-Nieves and Gómez2022). On the contrary, in the current group of elderly patients, survival was better and coincided with studies that applied early palliative care interventions (Zanghelini et al. Reference Zanghelini, Zimmermann and Souza de Andrade2018).
It is noteworthy that with our model, the referral time to palliative care was reduced (results not shown), therefore, improving the overall screening of potential candidates who could benefit from a GPCC approach is important. In accordance with existing literature (Allende-Pérez et al. Reference Allende-Pérez, Sánchez-Dávila and Peña-Nieves2021), we observed that elderly cancer patients present a highly complex status, and the implemented model can help to enhance and optimize care for these patients. The impact of our model in the medium and long term has yet to be assessed; hence, the retrospective nature of this study needs to be considered when interpreting our findings.
Conclusions
Geriatric palliative care plays an important role in cancer treatment. Elderly cancer patients are very frail and complex profile present multiple needs; thus, these patients require personalized care and a comprehensive treatment. A healthcare care model in which the elderly is the center of attention, which avoids old age, which prioritizes frailty screening, decreases the fractioning of care, impact on symptomatic control, facilitates early referrals and is based on a holistic and integrated approach could fulfill the gap of the unmet needs of these patients and their families.
An individualized treatment with a GPCS is a key element to assist the overall team treating elderly patients with cancer. However, more studies are required to establish an ideal healthcare model for these patients as palliative care is essential in this context.
Author contributions
Josafat Napoleon Sanchez-Davila: conception and design, manuscript writing, data collection, approval of final article; Emma L. Verástegui: design, manuscript writing, approval of final article; Adriana Peña-Nieves: data collection, analysis and interpretation of data, approval of final article; Silvia Allende-Perez: data collection, conception, approval of final article.
Funding
This research received no specific grant from any funding agency, commercial or not-for-profit sectors.
Competing interests
The authors declare none.
