Author:

Lisa Hutchinson

Abstract

Due to the progressive aging of the population, cancer in the older person has become an increasingly common global problem. In 1983, Rosemary Yancik and Paul Carbone in the USA at the National Institutes of Health organized a conference entitled “Perspectives on Prevention and Treatment of Cancer in the Elderly”, where it was underlined that while the cancer burden of the elderly was high and had increased over time, almost no data was available from clinical trials on elderly cancer patients. In Europe the first conference focused on geriatric oncology- the joint NCI-EORTC Consensus Meeting on Neoplasia in the Elderly- took place in 1990 and was held on San Servolo Island, in Venice. In this meeting it was underlined that, to describe the degree of fitness of elderly patients with cancer before therapy, the traditional oncological parameter, the Performance Status, was not sufficient to describe the condition of older cancer patients. This lead to the development of a tool for older cancer patients including the evaluation of all age associated conditions - the comprehensive Geriatric assessment (CGA). In 2000 a common interest in tailoring treatment for elderly cancer patients, and a focus on their needs, culminated in the founding of the International Society of Geriatric Oncology (SIOG) that unites clinical oncologists, geriatricians, nursing professionals and other healthcare professionals from around the world tasked with treating and caring for elderly patients with cancer. Thanks to the effort of investigators throughout the world, embattled but undeterred by the objection of a cautious establishment, SIOG has provided guidelines for the treatment cancer in the older person. In 2010, SIOG founded a dedicated journal for the cancer care and treatment of elderly patients, the Journal of Geriatric Oncology SIOG. Since 2017 a yearly SIOG Advanced Course in Geriatric Oncology has been held in Treviso, Italy, with participants coming from around the world, to attend sessions by oncologists for geriatricians, and by geriatricians for oncologists. Since a main concern of the utilization of the CGA is the time it takes to complete the test, several investigators have explored the value of using a shortened assessment to identify individuals in need of full assessment. SIOG has recommended among various testing systems the screening tool G8, developed in France. This country is a particularly good example for how to organize geriatric oncology research and clinical activity. Already in 2003, pilot units in geriatric oncology have been developed to cover the whole French territory and bring together oncologists and geriatricians to spark collaboration and improve management of geriatric cancer patients. An oncogeriatric interdisciplinary activity exists however only in a minority of high income countries and it is almost absent in those with a low one. On the oncology site, there is a lack of man power and often an inadequate information on CGA. On the geriatricians site the difficulties in recruitment into geriatrics are mainly due the complexities of the older patient and economical remuneration. Many geriatricians can be available to cooperate with oncologists in principle but may be involved with other multiple roles. Also the prejudice of ageism can lead to missing potential resources for the development of a generalized oncogeriatric approach.

What?

Geriatric oncology is not seen as a specialty field of oncology per se, but a way of approaching the care of elderly patients with cancer. When treating elderly patients with cancer, the problem lies in individualizing and tailoring care, says Riccardo Audisio, Professor of Surgery at Sahlgrenska University Hospital, Gothenburg. “Treating an elderly patient is easy, if you consider him a standard patient. But two disastrous outcomes can occur: You over-treat your patient, because you are not aware that the medical treatment or surgical procedure is more harmful than beneficial because of changes due to aging. Or you become hesitant and under-treat your older patient, because you believe him to be too old and frail to withstand treatment. The issue is to rule out the white and black areas, and navigate within the huge gray area to target the most accurate treatment.”

A common interest in tailoring treatment for elderly patients, and a focus on the needs of elderly cancer patients, arose in the 1980s and 1990s and culminated in the founding of the International Society of Geriatric Oncology in 2000. SIOG, based in Geneva, Switzerland, is a multidisciplinary society that unites oncologists, geriatricians, nursing professionals and other healthcare professionals from around the world tasked with treating and caring for elderly patients with cancer. In the past 20 years, SIOG – together with other initiatives in Europe and worldwide - has focused on strengthening capacities in geriatric oncology.

So what?

Treating elderly patients with cancer continues to be a challenge. However, the guidelines developed by SIOG and the increased interest in clinical studies in elderly cancer patients have improved the situation. “By promoting tailored care, we can avoid over-treatment and under-treatment – we have fewer operative deaths, less toxicity due to chemotherapy, and we more aggressively treat patients who gain most benefits”, says Audisio, a former president of SIOG. “Given that two out of three cancer patients are geriatric patients, this is a crucial role.” Looking back on 20 years of SIOG, and more than 30 years since his first paper on geriatric oncology, Dr. Silvio Monfardini– the second president in the history of SIOG – lists several achievements: “SIOG has become a reference point for geriatric oncology, and has promoted the importance of conducting studies in older patients – something which has been picked up also by other cancer societies. Last, but not least, the society’s journal has become a place to report and share information on cancer in elderly patients. This is a unique opportunity, as other cancer journals often do not see this as important.”

Context

“Cancer in the elderly: why so badly treated?” With this seminal paper (Fentiman, Tirelli, Monfardini et al., 1990), published in The Lancet, seven European oncologists put a spotlight on the poor treatment – and poor understanding – of elderly patients with cancer. They summarized the situation in stark words: “In current practice the elderly, disenfranchised as they are from entry to clinical trials, receive either untested treatments, inadequate treatment, or even none at all, at the whim of their clinician.” And their demand was clear: “The aim of good oncological practice is to balance probabilities of cure and toxicity, and chance of palliation with quality of life. Why should this not also apply to the elderly?”

Monfardini, one of the authors, recalls the context in which they felt this article was needed. “We started from the evidence that elderly patients were not treated in an optimal manner. Even before the article was published, there was an NIH conference on Cancer in the Elderly, and after our paper there was the joint NCI-EORTC Consensus Meeting on Neoplasia in the Elderly, held in Venice. Then we understood that there was a need for clinical studies, especially to address the situation in older patients.” With their Lancet paper, the authors sought to denounce the situation of cancer care for elderly patients in Europe, and called for a draft of clinical oncologists to cope with this situation. “This article had a shaking effect on the medical community. For us, this was the opportunity to prepare for future fights and cooperation among us in Europe on this subject”, says Monfardini.

While Monfardini and colleagues drew attention the issue of cancer in the elderly, they were not the first to highlight this issue. And oncologists weren’t even the first to pick this issue up, Monfardini adds: “It wasn’t by chance that the first person – in the US, and even for Europe – was not an MD. She was a medical sociologist: Rosemary Yancik. Yancik was the one who made a real effort to have a conference on this topic. Already in 1983, Rosemary Yancik and Paul Carbone at the National Institutes of Health organized a conference entitled “Perspectives on Prevention and Treatment of Cancer in the Elderly”, which reported that almost no data was available from clinical trials on elderly cancer patients (Yancik & Carbone, 1983). This was the beginning in the US. Rosemary Yancik stimulated this, she said: Here are the problems, with this conference, we need to start working on this, we need to organize this.”

However, not much was achieved to address this lack: 10 years later, Monfardini and Yancik pointed out in a jointly written paper that “a decade or so later, we are not much farther along a productive knowledge-generating pathway. We still know little about the effects of chemotherapy on the elderly (Monfardini & Yancik 1993).

Who what where how when (and why?)

More research activity on, and interest in, cancer in the elderly was witnessed in the 1990s. In Europe, the first conference focused on geriatric oncology took place in 1990, a few months after the publication of “Cancer in the elderly: why so badly treated?”. This joint NCI-EORTC “Consensus Meeting on Neoplasia in the Elderly” was held on San Servolo Island, in Venice. “At the first European conference, we came almost to the same conclusions as in the US”, Monfardini underlines. At the conference, attended by many European oncologists , a consensus was reached that “neoplasia in the elderly is an oncological time bomb” (Monfardini & Chabner, 1991).

Several areas of need were identified during the meeting, namely “to run properly designed protocols for the elderly”, that “frailty rather than age should be regarded as the primary constraint in the use of cancer therapy”, that “protocols for prospective controlled randomized trials should not be restricted by age” and “that to describe the degree of fitness of elderly patients with cancer before initiating therapy, the traditional oncological parameter of the Performance Status is not sufficient (Monfardini & Chabner, 1991). These outcomes and conclusions set the agenda for what was to come for geriatric oncology in Europe.

Further agenda setting was achieved by the afore mentioned paper jointly written by Monfardini and Yancik in 1993: “In our article, we further showed that the problem of older cancer patients was the same in the US and in Europe. We realized – even more – that the problem was almost universal in the developed countries.

In 1993, ESO offered an Advisory Report on Cancer Treatment in the Elderly to the European Community’s “Europe Against Cancer” programme (Monfardini, Aapro, Ferrucci et al., 1993). In this report, experts suggested funding priorities for improving cancer treatment in geriatric patients. They also formulated a message for the public, advising that two priorities should be added to the European Code against Cancer:

1. If you are an older person you should ask for a specialist’s opinion if it is suspected that you have a cancer. Treatments that can either cure or improve symptoms are available to all regardless of age.
2. Age is not itself a barrier to the successful treatment of cancer. Don’t hold back because of fear! Your life is too important!

However, no further action was taken following the report. “We were like prophets speaking in the desert. There was still no awareness of the problem”, says Monfardini.

Audisio recollects how age, and age alone, was frequently turned into a barrier to treatment.

“In 1999, I was a Visiting Professor at the University of Milan, and we were going around with the big professor, checking patients admitted overnight. And here comes this 85-year-old lady. She was doing yoga, she was going swimming regularly. And she had a very high rectal cancer, that could have been excised in a half-hour job. But because of her age, the big iconic professor said no. No, she’s not up for surgery, let’s treat her conservatively. So I followed this lady and it took her three years to die. But before, she had both ureters tended to, she had lots of pain. This was my personal approach to geriatric oncology. Where I said: damn, we really don’t know what we are doing.”

Towards a society for geriatric oncology

In the course of the 1990s, interest in the thematic area of geriatric oncology increased. In 1992, the first international conference on geriatric oncology was held in Buenos Aires. Also in this decade, the first textbooks on geriatric oncology were published in the US and in Europe, including by Ludovico Balducci, a US oncologist with Italian roots and a figurehead in geriatric oncology (Balducci et al., 1997).

The first geriatric oncology clinics were established in Europe in the 1990s, including at the Léon Bérard Cancer Center in Lyon, France and at the Aviano Cancer Center in Italy (Monfardini, Balducci, Overcash & Aapro, 2020). In Italy, a Cooperative Oncology Group focusing on geriatric oncology was launched, the “Gruppo Italiano di Oncologia Geriatrica” or GIOGer. And in 1992, the EORTC Neoplasia in the Elderly Study Group was launched, with Monfardini as Chairman. The goal of this committee was to facilitate enrolling elderly cancer patients in clinical trials. However, success was limited, as Monfardini points out: « We were not allowed to look into protocols, so unfortunately, very little was achieved through this study group ».

Oncologists and geriatricians with an interest in cancer treatment in elderly patients continued to unite at international conferences, in Rome, Geneva and Tampa (Mc Neil,2013). By 2000, growing interest in the field of geriatric oncology led to the formation of the first international society focused on this topic, the International Society of Geriatric Oncology (SIOG). Although founded in 2000, SIOG was officially registered as a not-for-profit organization under Swiss law in 2012.

A key figure in the formation of SIOG was Matti Aapro, as Monfardini points out. “From a historical and practical point of view, Aapro was a key person. He is the most international man I know, and for years he has been the pivot of the society.” Since the Society’s foundation, the presidency has alternated between oncologists based in Europe and in the US; the current president, Ravindran Kanesvaran, based in Singapore, is the first SIOG president located in Asia.

“SIOG was founded in Europe, and we managed to set up a network that glues in interested collaborators, first from the US, and now from Japan, Malaysia and other Asian countries”, Audisio, president of SIOG from 2010 to 2012, points out. “I would also stress that SIOG is an interdisciplinary society”, Audisio says, pointing especially towards the SIOG Advanced Course in Geriatric Oncology in Treviso, Italy. “Participants come from around the world, to attend sessions by oncologists for geriatricians, and by geriatricians for oncologists – to have this intermingling.”

In 2010, SIOG founded a dedicated journal for the cancer care and treatment of elderly patients, the Journal of Geriatric Oncology.

How to distinguish fit from frail?

An early guideline published by SIOG in 2005 concerned the use of the Comprehensive Geriatric Assessment (CGA) in elderly cancer patients, recommending that geriatric assessments are used to identify health and functional status issues in older cancer patients (Extermann, Aapro, Bernabei, et al., 2005). The assessment of older patients – both within and outside clinical trials – has been one of the focus points of geriatric oncology, a field concerned with patients with many co-morbidities aside from cancer, as well as polypharmacy.

Already in 1996, Monfardini and colleagues validated a multidimensional assessment used in patients over the age of 70 (Monfardini, Ferrucci, Fratino et al, 1996). In 1998, Martine Extermann – eventually also a president of SIOG – reviewed the outcome of patients who had undergone a comprehensive geriatric assessment (CGA) and showed that a CGA was feasible and necessary for older patients with cancer. The CGA is a multidisciplinary evaluation, which identifies medical, social and functional needs.

Audisio was one of the researchers who continued to investigate the usefulness of CGA for cancer patients, particularly for surgical patients. “After my shocking encounter with our big professor, I wanted to see whether there was any reason to avoid operating on older patients”, Audisio recalls. “So I pulled together literature for gastroesophageal cancer and colorectal cancer. But realizing my bias – only looking at fit patients – I saw that we needed to put down some evidence surrounding the CGA.” In 2002, in a study by GIOGer, Audisio and others found that the CGA adds information on the fitness of older patients with cancer ( Repetto, Fratino, Audisio et al. 2002). And in 2005, Audisio and colleagues published a study on the preoperative assessment of surgical risk in oncogeriatric patients, a further assessment tool focused specifically on surgical patients and their outcomes ( Audisio, Ramesh, Longo et al, 2005). « But as a physician, he says, I never could assess my surgical patients with a CGA, that would take too much time. I realized I needed something quicker, something that patients could fill in while waiting ». The value of assessment tools was convincingly proven with the GOSAFE study on surgically treated colorectal cancer patients aged >70 years: frailty assessment was performed and outcomes, including Quality of Life, were recorded postoperatively. Frailty Recovery was defined as a combination of Activity of Daily Living ≥5 + Timed Up & Go test <20 seconds + MiniCog >2. The majority of older patients experienced good Quality of Life and stay independent after colorectal cancer surgery. Predictors for failing to achieve these essential outcomes are now defined to guide patients' and families' preoperative counseling (Montroni , Ugolini , Saur et al, 2023)

A review of screening tools and the CGA led to an update of the SIOG recommendations in 2015 (Decoster, K Van Puyvelde , S Mohile, et al. , 2015). Audisio recalls: « This was a comparison between outcomes reached in patients who were screened using screening tools, and in patients who had a full geriatric assessment. And the outcome is the same: screening tools are very good in picking up those patients who we need to pick up. So this spares us a lot of time ».

« The chief of INCa in France asked a simple question: how can we decide on treatment, without losing 45 minutes to an hour on a multi-dimensional assessment done by a geriatrician? », remembers Monfardini. « So in Bourdeaux, Pierre Soubeyran developed the G8, a series of questions that can be answered in 10 minutes or less » (Soubeyran, Bellera, Goyard et al., 2011).

In practice, these screening tools help to identify patients who might need optimized management, Audisio points out. “We used to think that we would need the geriatrician all over. Fortunately, that is not the case – we only need a geriatrician for about one in 5 geriatric patients. These screening tools help you identify the ones that you pass to the geriatrician.” Currently, researcher are investigating the use of assessment tools as a way to optimize geriatric patients’ status pre-treatment, and so improve outcomes. Cancer in the elderly has come a long way since 1990. SIOG has issued nearly 40 guidelines on how to manage geriatric cancer patients; and from 2014 onwards, a series of studies in older patients evaluated with geriatric assessment tools have been published – with the first one, in patients with Chronic Lymphocytic Leukemia, carried out in Europe

For Monfardini, France is a particularly good example for how to organize geriatric oncology research. Already in 2003, 15 pilot units in geriatric oncology were established, the so-called UPCOG. These units, later expanded to 24, cover the whole French territory and bring together oncologists and geriatricians to spark collaboration and improve management of geriatric cancer patients. “This is a beautiful example”, Monfardini points out. “The UPCOG insist on interdisciplinary in the research or research protocol. This happened because special funding was available, and to me, this is the best example on how there was an impulse and support to such an activity [in geriatric oncology] (Balducci & Monfardini, 2022).

France is in a privileged position but Monfardini stresses also the fact that an oncogeriatric interdisciplinary activity exists only in a minority of high income countries and it is almost absent in those with a low one. Considering topics, sessions and tracks of the main meetings and conferences of the major Oncological Societies in Europe and worldwide, USA excluded, little attention has so far been payed to the problem of cancer in the elderly. Again, with the exception of the USA, the major cooperative groups, for example the EORTC in Europe, have only dedicated a marginal attention to the research issue of cancer in the elderly. Despite major shortcomings professionals interested in geriatric oncology, as already underlined, have taken a number of important initiatives to highlight the benefits of this particular activity. In spite of these efforts, the management of cancer in the older population is still encountering several important and generalized pitfalls (Monfardini, Perrone & Balducci, 2023).

The main obstacle is the grossly inadequate number of geriatricians and clinical oncologists necessary to an integrated care of the expanding aging population. Beside that, on the oncology site, the main focus of training is to provide a rapid solution of the oncological problems rather than to be involved in the complex, time consuming care of an older person. Lack of information on CGA is also a problem. Also Geriatrician’s tools and know-how are often perceived ambiguously by clinical oncologists. On the geriatricians site the difficulties in recruitment into geriatrics are mainly due the complexities of the older patient and economical remuneration. Many geriatricians can be available to cooperate with oncologists in principle but may be involved with other multiple roles and suffer from a time constraint due to the overwhelming number of elderly cancer patients. Geriatricians may also feel confined to the periphery of the organization of cancer treatment (Monfardini, Perrone & Balducci, 2023).

Also the prejudice of ageism can lead to missing potential resources for the development of a generalized oncogeriatric approach. Ageist beliefs at the society level can lead to providing inadequate societal resources for the care of older patients who may be considered disposable (Monfardini, Perrone & Balducci, 2023). But there is still room for contributions to geriatric oncology. “We have set the foundations for improvements”, Audisio points out, “My target has never been to revolutionize what’s going on in a day, but to promote a culture where good quality, tailored treatments and individualized care is the point.”

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