Emergency presentation is a common consequence of cancer and complications of its treatment, represents an important proportion of new presentations of previously undiagnosed malignancy, and is associated with poor survival outcomes and patient experience, and poorly coordinated care. The recent development of acute oncology services in the U.K. aims to improve patient safety, quality of care, and the coordination of care for all patients with cancer who require emergency access to care. Prompt management coordinated by expert teams and access to protocol-driven pathways have the potential to improve patient experience and drive efficiency when services are fully established.
Keywords: Acute oncology, Emergency cancer care, Cancer outcomes, U.K. oncology
Abstract
Remarkable progress has been made over the past decade in cancer medicine. Personalized medicine, driven by biomarker predictive factors, novel biotherapy, novel imaging, and molecular targeted therapeutics, has improved outcomes. Cancer is becoming a chronic disease rather than a fatal disease for many patients. However, despite this progress, there is much work to do if patients are to receive continuous high-quality care in the appropriate place, at the appropriate time, and with the right specialized expert oversight. Unfortunately, the rapid expansion of therapeutic options has also generated an ever-increasing burden of emergency care and encroaches into end-of-life palliative care. Emergency presentation is a common consequence of cancer and of cancer treatment complications. It represents an important proportion of new presentations of previously undiagnosed malignancy. In the U.K. alone, 20%–25% of new cancer diagnoses are made following an initial presentation to the hospital emergency department, with a greater proportion in patients older than 70 years. This late presentation accounts for poor survival outcomes and is often associated with poor patient experience and poorly coordinated care. The recent development of acute oncology services in the U.K. aims to improve patient safety, quality of care, and the coordination of care for all patients with cancer who require emergency access to care, irrespective of the place of care and admission route. Furthermore, prompt management coordinated by expert teams and access to protocol-driven pathways have the potential to improve patient experience and drive efficiency when services are fully established. The challenge to leaders of acute oncology services is to develop bespoke models of care, appropriate to local services, but with an opportunity for acute oncology teams to engage cancer care strategies and influence cancer care and delivery in the future. This will aid the integration of highly specialized cancer treatment with high-quality care close to home and help avoid hospital admission.
Implications for Practice:
Emergency presentations of cancer patients to health care services can be associated with high risks and poor outcomes. Systematic approaches are described to create best practice for these patients based on expert teams and careful organization of services in all hospitals. These approaches, called “acute oncology” in the U.K., may improve care and avoid unnecessary deaths.
Introduction
Cancer remains a major cause of morbidity and mortality on a global scale. Worldwide in 2012, 14.1 million adults were diagnosed with cancer and there were 8.2 million deaths due to cancer with greater than 60% of cancer deaths occurring in less-well-developed regions of the world [1]. In the U.K. alone, there are 325,000 new cases of cancer diagnosed annually, with 159,000 deaths contributing 28% of all deaths every year. Over the last 10–20 years, there has been an inexorable increase in the number of patients receiving systemic anticancer chemotherapy (SACT); this now accounts for approximately £1 billion in expenditures annually in the U.K. alone, demonstrating the financial burden of excellent cancer care.
Although the increasing delivery of SACT has resulted in improved outcomes for patients with cancer, it has also resulted in an increasing burden of cancer treatment complications. The National Confidential Inquiry into Patient Outcomes and Death (NCEPOD) published in 2008 in the U.K. highlighted concerns regarding the quality and safety of care for patients who died within 30 days of receiving SACT [2]. The inquiry was set up to audit the care pathways for this vulnerable group of patients with cancer. In only 35% of patients was the care deemed to be acceptable. In 49% of patients, care was deemed to be less than optimal, with factors being identified that related to both the organization of emergency care as well as the specific care delivered by each institution. The report highlighted the fragmented care pathways faced by many patients, with many interfacing with multiple institutions and departments within a given institution. In the report, 42% of all patients with cancer were admitted under general medicine rather than to a specialist oncology ward, with 43% of these patients recorded as having grade 3 or 4 SACT-related toxicity on admission before death. Eighty-six percent of patients were treated with palliative intent, with almost half on their second or subsequent line of SACT; 15% of patients were not admitted to the organization where their SACT was administered.
It is recognized that the NCEPOD report was an important publication in that it highlighted deficiencies in the management of patients receiving SACT within the U.K., and U.K. cancer leaders extensively reviewed the report and felt that a response to the findings was warranted. It is also recognized that the report had its limitations, including a lower overall return rate for all questionnaires and case notes requested compared with previous NCEPOD studies, as well as an acknowledgment that although the patients in the study were not representative of patients receiving SACT as a whole, the findings needed to lead to a continuing debate on how to improve services to patients with cancer. The problems identified in this U.K. report may be international problems and it is possible that they are relevant to other health-care systems worldwide.
As a result, in response to this report and concerns raised by national pharmacy alerts, the National Cancer Action Group (NCAG) was formed to address how care should be delivered to improve the outcomes of emergency presentation of patients with cancer, and to address the key issues that needed to be improved in the organization of care to improve the overall patient experience [3]. Examples of three cases that may take these approaches are given as supplemental online cases 1–3.
Acute Oncology Services in the U.K.
The 2009 NCAG report “Chemotherapy services in England: Ensuring quality and safety” led to the concept of acute oncology, with a key recommendation that every Acute Hospital Trust (the management unit for one or more hospitals working together) with an emergency department should establish an Acute Oncology Service (AOS). The report highlighted the highly variable models of oncology delivery throughout the U.K. and the not uncommon dissociation of oncology expertise away from acute care pathways. The authors described an AOS as being led by consultant oncologists with the support of oncology nurse specialists and being tasked with bringing together the expertise from palliative care and hematology disciplines, and emergency medicine, general medicine, and general surgery to ensure the rapid identification and prompt management of all patients who present with severe complications following chemotherapy or as a consequence of their known cancer.
Importantly and never previously described, NCAG also recommended the potential lead role for an AOS in the coordination of the care of patients who present to the emergency department with previously undiagnosed cancer. National Cancer Intelligence Network data indicate that approximately 25% of all new cancers diagnosed per year in England are diagnosed following an emergency admission to the hospital, with lung, pancreas, and malignant brain tumors forming the largest group diagnosed in this way. This group of patients often presents to the hospital acutely unwell, via a wide range of routes, including the emergency department, and with a constellation of symptoms, and are then subsequently found to have cancer. Such patients often experience delayed referral to oncology and palliative care services. Inevitably, the survival for this group of patients is far worse compared with those who are referred by their general practitioner directly to elective nonemergency services via conventional suspected-cancer referral pathways. This is because such patients present with advanced disease and with poor performance status, and often, particularly in the elderly, with multiple comorbidities.
National Cancer Intelligence Network data indicate that approximately 25% of all new cancers diagnosed per year in England are diagnosed following an emergency admission to the hospital, with lung, pancreas, and malignant brain tumors forming the largest group diagnosed in this way.
Acute oncology is underpinned by a number of core principles that promote education, awareness, and early access to specialist oncology input, as well as a more integrated way of working among acute specialties within hospital trusts. In these models, early specialist review must be combined with strong leadership and innovative service developments that will improve the safety and quality of emergency cancer care that has been less than satisfactory in the past. The number and type of acute oncology emergency admissions are highly dependent on local service configuration and reflect the role of an individual hospital trust as either an acute district general hospital, where patients admitted acutely with complications related to their cancer and its treatment are often admitted via the emergency department to general medical admissions units and managed acutely by nononcology specialists, or a fully integrated cancer center with direct admission for all patients to oncology specialist wards with appropriate local acute medical and surgical support, as required, or a standalone cancer center that lacks acute medical and surgical support. Despite these differences, for each of these services, the core principles remain the same; however, the models of care may appear very different and will be developed to meet the specific local needs. It was also recognized that these services would need commissioning locally, with a need for additional oncologists and specialist nurses within hospital trusts to deliver an efficient and effective AOS.
Published data on acute oncology patterns and workload remain sparse. In 2006–2007, there were 273,000 emergency admissions in England with a diagnosis of cancer, which represented a 30% increase from 1997–1998 [2]. This roughly equates to 750 emergency admissions each day across England, so that a typical hospital trust may have 5 emergency admissions with cancer per day. Furthermore, it is not uncommon for an individual patient to experience several emergency cancer admissions during their cancer journey. A 12-month report from a newly formed regional cancer network AOS identified 3,013 new patient admissions across 7 hospitals from a population of 2.3 million, equating to approximately 500 admissions per hospital emergency site [4]. Fifty-one percent of admissions were due to complications of cancer, 30% were considered complications of treatment, and 19% were new diagnoses of malignancy. Lung cancer represented the most common primary tumor diagnosis. The average hospital length of stay for inpatient cancer admissions varies nationally and ranged from 5.1 to 10.1 days between regions in 2008–2009. Improving average length of stay nationally to that of the regions in the best performing quartile could lead to a significant reduction in bed days and to significant cost savings in the National Health Service (NHS) [5].
Solutions and options for acute oncology in England require effective leadership and a clear understanding of pathways for patients with cancer within cancer networks but also within individual hospital trusts. The different models that will need to be developed depending on local service configurations may be very different nationally, but all will share the common themes of triage, cancer alerts, early specialist review, and defined inpatient pathways; areas that have all been highlighted by the NHS improvement, transforming inpatient care program [6] (Panel 1).
Acute oncology services in the U.K. have evolved along differing models dependent on local resource and service design. The proposed requirement for consultant oncology leadership in every hospital has posed logistical and financial problems compounded by the limited number of available trained oncologists. These challenges have been highlighted by national AOS peer review of the 183 services, with a median range of 50% fulfilling nationally agreed peer-review measures that include team structure, training, and specific aspects of emergency cancer pathways, including neutropenic sepsis and spinal cord compression [7]. The report recognizes many examples of innovative practices but raises concerns about the extent of oncologist engagement in many parts of England. Despite the real challenges, an increasing number of publications have identified the potential benefits of an AOS in terms of reduced hospital length of stay, improved patient experience, and efficiency savings [4, 8].
International Experience
Cancer is a leading cause of morbidity and mortality in North America. In 2012, approximately 186,400 new cases of cancer and 75,700 cancer deaths were expected in Canada [9], and 1,638,910 new cases of cancer and 577,190 cancer deaths were expected in the U.S. [10]. In both countries during the last decade, there has been significant interest in reforming health-care delivery at both the policy and practice levels because of concerns regarding quality of care in a number of areas [11–16]. Delivery and payment of cancer services in Canada and the U.S. are significantly different. Most health services in Canada, including cancer care, are paid for publically, with legal residents entitled to receive necessary medical care without copayment, and most Canadian provinces have elected to develop provincial agencies, such as Cancer Care Ontario [17] or the British Columbia Cancer Agency [18], to organize and deliver their cancer services. This has led to a centralized approach to delivery of cancer care, with regional cancer centers and their affiliated institutions delivering the vast majority of specialized care such as chemotherapy and radiotherapy. In the U.S., however, health care, including cancer care, is paid for by a number of different systems, including public programs (e.g., Medicare for those over age 65 years, Medicaid for the poor) and also private insurance plans often obtained as part of an employment package. Most cancer care in the U.S. is delivered through a fee-for-service model, with care being delivered largely in community-based settings by private practitioners. Although this enables patients to choose from a wide range of care providers, it can often result in fragmented care across many sites.
Similar to the U.K., one of the biggest challenges facing cancer care delivery in North America is the management of acute complications of cancer treatments and complications of the cancer itself, especially in those patients with advanced, often incurable disease. A Canadian study found that 84% of patients who died of cancer in Ontario between 2002 and 2005 made 194,017 visits to the emergency department in the last 6 months of life, and that 40% of the visits were made in the last 2 weeks of life [19]. Patients receiving chemotherapy for early-stage breast cancer have also been shown to have frequent visits to the emergency department and acute admissions to hospital [20, 21]. These studies highlight the need for developing novel models of delivering acute oncology for patients with cancer in North America. Currently, management of acute oncology issues has focused largely on the following three areas: use of preventive strategies, patient education, and telephone support. Guidelines have been developed by the American Society of Clinical Oncology that recommend appropriate antiemetics for prevention of treatment-induced nausea and vomiting [22] and prophylaxis for febrile neutropenia [23]. Similar to the process in the U.K., all patients are educated in the management of treatment toxicities by either medical or nursing staff involved in their care, with some centers developing formal chemotherapy classes that provide patients and their caregivers with information regarding potential side effects and their management. The majority of centers provide access to telephone advice for urgent care issues; however, fewer centers have the capacity to see patients acutely in clinics or provide advice outside clinic hours. For specific acute oncology issues, such as febrile neutropenia, protocols for management of low-risk patients in the outpatient setting have been developed, but it is difficult to know their uptake nationally [24].
In the U.S., a concept of the oncology medical home is being developed; the idea behind the oncology medical home arose from the patient-centered medical-home program created on the basis of National Committee for Quality Assurance standards [25]. This model assumes greater responsibility by the oncology team for disease management and coordination of care, and more active patient engagement, in a bid to improve not only the quality of care delivered but also patient satisfaction while still optimizing care efficiency. This, in turn, should lead to cost savings; preliminary evaluations in the primary care setting show promising results [26, 27]. Several oncology groups around the U.S. have adopted this model of care and as experience with it increases, data will become available evaluating its use.
End-of-life care is another major issue in oncology in North America and studies have found that a significant proportion of patients with end-stage cancer receive aggressive care at the end of life defined as chemotherapy close to death, admissions to hospital and intensive care units within the last few weeks of life, and underuse of hospice services [28, 29]. Recent studies have shown significant benefits to early introduction of palliative care and better end-of-life care in terms of survival [30], quality of life [31], and aggressiveness of care in patients with end-stage cancer [32]. In response, both Canada and the U.S. have identified end-of-life care as an important target for quality improvement, with significant efforts in both countries to improve quality of end-of-life care that focuses on systematic and comprehensive symptom management [33] and on integration of early palliative care input in a standardized way [34].
In recent years, one of the main ways in which Canada and the U.S. have looked to improve the quality of cancer care and its delivery has been through the use of quality measurement to drive change. In some provinces in Canada, there has been public reporting of cancer care quality since 2005. In Ontario, Canada’s most populous province, gaps in care identified through measurement are being used to drive quality improvement, particularly in relation to access to services. In the U.S., a number of cancer organizations have developed formal quality-measurement systems, including the American Society of Clinical Oncology’s Quality of Oncology Practice Initiative (QOPI) [35] and the American College of Surgeons’ Commission on Cancer Rapid Quality Reporting System [36]. The QOPI, originally developed by a group of community oncologists as a means of evaluating adherence with care processes, continues to grow and evolve, and is currently being used by approximately 10% of American oncology practices [37]. Although the majority of these quality reporting programs historically have been voluntary, with the passing of the Accountable Care Act in 2010, it is now a requirement to participate for many involved in providing cancer services. Overall, cancer care in Canada and the U.S. is expensive and often unable to respond to the acute needs of patients with cancer across the continuum of care. Like in the U.K., novel models of cancer care that promote patient engagement and a multifaceted approach to care are being developed in North America and are likely to change the way acute problems are managed in patients with cancer in the near future.
In contrast, in Australasia, the biggest challenges to offering acute cancer services come from the widely dispersed populations in the two countries; but similar to the U.K. and North America, increasing oncology care is required for the growing population, in particular the elderly, together with the ever-increasing complex, effective therapies. Australia has 22.7 million people spread over 7.66 million km2 (approximately 3 people per km2). The population is widely spread, often near the coasts, with some areas, such as New South Wales, being very densely populated and other areas, such as Northern territory, significantly less so [38]. New Zealand has 4.2 million people, spread over 0.27 million km2 (approximately 15 people per km2), which is similar in area to the U.K. (approximately 260 people per km2) [39].
Both Australia and New Zealand have demonstrated inequities of outcome, which can be explained partly because of the dispersed rural and remote populations, but are especially associated with indigenous peoples, including New Zealand Maori and Pacific peoples [40–43]. These inequities come from a lack of prompt referral with a suspected new cancer diagnosis and for adjuvant therapy and acute problems, access to specialist cancer units, access to acute care for therapy complications, and also access to specialist palliative care. In 2006, the Clinical Oncology Society of Australia (COSA) mapped cancer services in regional and rural Australia [44], identifying 161 regional hospitals administering chemotherapy, with a 98% response rate. Only 21% had a resident medical oncologist; 7%, a radiation oncology unit; 6%, a surgical oncologist; 24%, a palliative care specialist; and 39%, a dedicated oncology counseling service. In only 61% of hospitals was chemotherapy being given by appropriately trained chemotherapy nurses. This situation prompted national cancer control initiatives in Australia, followed by New Zealand, and led to the Cancer Council of Australia, together with COSA and the National Cancer Control Initiative, making 12 recommendations for “Optimising Cancer Care in Australia,” which included integrated multidisciplinary care, improved palliative care, better access to clinical trials, and improvements in radiation, among others [45].
In New Zealand, the “New Zealand Cancer Control Strategy Action Plan 2005-2010” was produced and led to establishment of the Cancer Control Council in 2005 (Cancer Control New Zealand since 2010 and the four regional cancer networks in 2006) [46]. There are six cancer centers and each has clinician-initiated multidisciplinary meetings, provides both chemotherapy and radiotherapy services, and manages acute problems related to cancer or treatment complications. These centers are also linked to several peripheral centers where chemotherapy, but not radiotherapy, is administered. Some of these have resident medical oncologists and others have visiting medical and/or radiation oncologists. In general, acute problems related to either the cancer itself or complications of treatment affecting peripheral patients are managed by their general practitioner or at their local hospital, not the linked cancer center. Specialist nurses in the peripheral hospitals facilitate the support for managing care pathways, such as neutropenic sepsis, and acute referrals with cancer- or treatment-specific problems, but there remains considerable variation in the support for patients in the community, depending on where they live.
In remote areas of Australia, acute oncology is delivered by improving the skills of nurses and nonspecialist doctors through programs such as educational workshops about chemotherapy [47]. Telehealth is increasingly being used for patient assessment, multidisciplinary discussions, and education [48]; radiologic investigations are undertaken locally in remote centers in Australia, and patients have their radiotherapy planning done locally by the visiting radiation oncologists to provide patient-centered care where possible [42, 49]. Despite this progress, deficiencies in care still persist, including lack of travel support and shortage of visiting oncologist time, and cancer survival in rural and remote areas in Australia still lags behind that of patients in metropolitan centers.
Acute oncology services in Australasia have been transformed over the last decade with equity of access to specialist oncological services and an increased focus on patient-centered services being at the center of the improvements. There is still significant variation in cancer services between states and networks and, moving forward, significant challenges remain in serving not only the more remote populations but also the needs of the increasing and aging populations with greater comorbidity.
Conclusion
Acute oncology represents a major shift in the direction of oncology from an ever-greater need for subspecialization and personalized medicine back toward a need to deliver unplanned oncology care using basic cross-cutting principles that are relevant to all patients with cancer, particularly when they initially present with suspected cancer, to ensure timely specialist input to enable appropriate investigation and further management. The development of acute oncology services internationally will vary greatly and what works for one health-care system will not necessarily work for another, potentially leading to significant differences in the way these services are developed moving forward; but they will have the same underlying principles of providing excellent care for such patients. Evidence, albeit largely anecdotal, suggests that acute oncology has certainly been warmly welcomed by U.K. NHS Hospital Trusts and general medical colleagues and is already leading not only to improved care and coordination but also a reduction in length of hospital stay and efficiency savings. It is already recognized that acute oncology will affect the way cancer medicine is delivered throughout the world as outlined in this review.
Acute oncology represents a major shift in the direction of oncology from an ever-greater need for subspecialization and personalized medicine back toward a need to deliver unplanned oncology care using basic cross-cutting principles that are relevant to all patients with cancer, particularly when they initially present with suspected cancer, to ensure timely specialist input to enable appropriate investigation and further management.
The challenge of acute oncology provides excellent opportunities for acute oncology teams worldwide to engage and influence cancer strategy. This will allow the integration of highly specialized cancer treatment alongside local delivery, and will help avoid admissions. Acute oncology teams are likely to play a key role in service development alongside partner organizations in both secondary and primary care. Future care will require greater contingency planning for emergency care and greater access to information and advice to support patients and professionals. This should enable early detection and management of cancer complications such as suspected febrile neutropenia, the management of which might incorporate, for example, community-based services that allow rapid assessment of neutrophil count, risk stratification, and early antibiotic use, with the most serious cases perhaps requiring hospital intervention. As the population in the developed world increases in age, acute oncology services will need to be able to handle the older population and, thus, the likely increase in diagnostic and clinical events in this population both in hospital and in the community.
Many patients will continue to require assessment by oncology teams despite enhanced patient information and community support. Access to timely outpatient clinics or for review by oncology teams in their treatment facilities will become ever-more relevant worldwide. Increasingly, these outpatient services will need to incorporate extended hours of work and provide facilities to support ambulatory care and outpatient procedures that have historically required inpatient stay. These services will need to integrate and work alongside existing acute medical and palliative care services as a means of maximizing opportunities for efficiency and teamwork, thus avoiding acute cancer services working in isolation. Capacity will continue to be a significant challenge worldwide and will only be achieved by developing allied work streams in other areas of cancer care, such as community chemotherapy and devolved follow-up for low-risk patients.
Clinicians involved in the development and delivery of acute oncology will have a critical role to play in delivering training and education to all health-care professionals who respond to patients with cancer and acute cancer needs. Solutions will include generic training at all levels of education and also the development of innovative e-learning packages and the evolution of acute oncology staff with the responsibility of cascading information and principles of care to the wider health-care community. The changing way we look to manage acutely ill patients with cancer may lead to the emergence of a much-needed research and evidence base in this orphan area. High-quality research in the field of acute oncology is severely lacking and will pose a significant challenge in protocol development and delivery of acute oncology worldwide, but it remains an important future direction for acute oncology in the developed world.
The increasing incidence of cancer, alongside the aging population and the explosion of new therapies, is leading to larger numbers of patients who are fit for treatment. This will continue to challenge cancer services worldwide. Acute oncology represents a key development that will remain at the forefront of cancer strategy now and in the future. The key to successful acute cancer care moving forward lies in the ability of acute oncology to develop care pathways that educate patients and professionals, increase and enhance opportunities for community and specialist palliative care, and provide speedy access to advice and clinical review for acutely unwell patients with cancer 24 hours a day and 7 days a week.
See http://www.TheOncologist.com for supplemental material available online.
Supplementary Material
Author Contributions
Conception/Design: Alison Young, Ernie Marshall, Monika Krzyzanowska, Bridget Robinson, Sean Brown, Fiona Collinson, Jennifer Seligmann, Afroze Abbas, Adrian Rees, Daniel Swinson, Helen Neville-Webbe, Peter Selby
Provision of study material or patients: Alison Young, Ernie Marshall, Monika Krzyzanowska, Bridget Robinson, Sean Brown, Fiona Collinson, Jennifer Seligmann, Afroze Abbas, Adrian Rees, Daniel Swinson, Helen Neville-Webbe, Peter Selby
Collection and/or assembly of data: Alison Young, Ernie Marshall, Monika Krzyzanowska, Bridget Robinson, Sean Brown, Fiona Collinson, Jennifer Seligmann, Afroze Abbas, Adrian Rees, Daniel Swinson, Helen Neville-Webbe, Peter Selby
Data analysis and interpretation: Alison Young, Ernie Marshall, Monika Krzyzanowska, Bridget Robinson, Sean Brown, Fiona Collinson, Jennifer Seligmann, Afroze Abbas, Adrian Rees, Daniel Swinson, Helen Neville-Webbe, Peter Selby
Manuscript writing: Alison Young, Ernie Marshall, Monika Krzyzanowska, Bridget Robinson, Sean Brown, Fiona Collinson, Jennifer Seligmann, Afroze Abbas, Adrian Rees, Daniel Swinson, Helen Neville-Webbe, Peter Selby
Final approval of manuscript: Alison Young, Ernie Marshall, Monika Krzyzanowska, Bridget Robinson, Sean Brown, Fiona Collinson, Jennifer Seligmann, Afroze Abbas, Adrian Rees, Daniel Swinson, Helen Neville-Webbe, Peter Selby
Disclosures
The authors indicated no financial relationships.
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