Download as docx, pdf, or txt
Download as docx, pdf, or txt
You are on page 1of 25

Lung Cancer 150 (2020) 221–239

Contents lists available at ScienceDirect

Lung Cancer
journal homepage: www.elsevier.com/locate/lungcan

Review

European Cancer Organisation Essential Requirements for Quality Cancer


Care (ERQCC): Lung cancer
Thierry Berghmans a, 1, Yolande Lievens b, 1, Matti Aapro c, Anne-Marie Baird d, Marc Beishon e,*, Fiorella
Calabrese f, Csaba D´egi g, Roberto C. Delgado Bolton h, Mina Gaga i, Jo´zsef Lo¨vey j, Andrea Luciani
k
, Philippe Pereira l, Helmut Prosch m, Marika Saar n, Michael Shackcloth o,
Geertje Tabak-Houwaard p, Alberto Costa q, Philip Poortmans r
a
European Organisation for Research and Treatment of Cancer (EORTC); Thoracic Oncology Clinic, Institut Jules Bordet, Brussels, Belgium
b
European Society for Radiotherapy and Oncology (ESTRO); Radiation Oncology Department, Ghent University Hospital, Belgium
c
European Cancer Organisation; Genolier Cancer Center, Genolier, Switzerland
d
European Cancer Organisation Patient Advisory Committee; Central Pathology Laboratory, St James’s Hospital, Dublin, Ireland
e
Cancer World, European School of Oncology (ESO), Milan, Italy
f
European Society of Pathology (ESP); Department of Cardiac, Thoracic, Vascular Sciences and Public Health, University of Padova Medical School, Padova, Italy
g
International Psycho-Oncology Society (IPOS); Faculty of Sociology and Social Work, Babes-Bolyai University, Cluj-Napoca, Romania
h
European Association of Nuclear Medicine (EANM); Department of Diagnostic Imaging (Radiology) and Nuclear Medicine, San Pedro Hospital and Centre for
Biomedical Research of La Rioja (CIBIR); University of La Rioja, Logron˜o, La Rioja, Spain
i
European Respiratory Society (ERS); 7th Respiratory Medicine Department, Athens Chest Hospital Sotiria, Athens, Greece
j
Organisation of European Cancer Institutes (OECI); National Institute of Oncology, Budapest, Hungary
k
International Society of Geriatric Oncology (SIOG); Medical Oncology, Ospedale S. Paolo, Milan, Italy
l
Cardiovascular and Interventional Radiological Society of Europe (CIRSE); Clinic for Radiology, Minimally-Invasive Therapies and Nuclear Medicine, SLK-Kliniken,
Heilbronn, Germany
m
European Society of Radiology (ESR); Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Austria
n
European Society of Oncology Pharmacy (ESOP); Tartu University Hospital, Tartu, Estonia
o
European Society of Surgical Oncology (ESSO); Department of Thoracic Surgery, Liverpool Heart and Chest Hospital, Liverpool, United Kingdom
p
European Oncology Nursing Society (EONS); Deventer Hospital, Deventer, Netherlands
q
European School of Oncology (ESO), Milan, Italy
r
European Cancer Organisation; Iridium Kankernetwerk and University of Antwerp, Wilrijk-Antwerp, Belgium

ARTICLEINFO
ABSTRACT
Keywords:
Lung cancer European Cancer Organisation Essential Requirements for Quality Cancer Care (ERQCC) are written by experts
Quality representing all disciplines involved in cancer care in Europe. They give patients, health professionals, managers
Cancer centre and policymakers a guide to essential care throughout the patient journey.
Cancer unit Lung cancer is the leading cause of cancer mortality and has a wide variation in treatment and outcomes in
Europe
Europe. It is a major healthcare burden and has complex diagnosis and treatment challenges. Care must
Care pathways
only be carried out in lung cancer units or centres that have a core multidisciplinary team (MDT) and an
Multidisciplinary
Organisation of care
extended team of health professionals detailed here. Such units are far from universal in European
Audit countries.
Quality assurance To meet European aspirations for comprehensive cancer control, healthcare organisations must consider
Patient-centred the requirements in this paper, paying particular attention to multidisciplinarity and patient-centred pathways
Multidisciplinary team from diagnosis, to treatment, to survivorship.
Patient information
Health inequalities
Essential requirements
Guidelines
Healthcare system

* Corresponding author.
E-mail address: marcbeishon@icloud.com (M. Beishon).
1
Joint first authors: T. Berghmans and Y. Lievens contributed equally to this article.

https://doi.org/10.1016/j.lungcan.2020.08.017
Received 24 August 2020; Accepted 26 August 2020
Available online 4 September 2020
0169-5002/© 2020 Published by Elsevier B.V.
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
Lung cancer is the leading cause of cancer death globally [7]. It
1.• Introduction: the need for quality frameworks is predominantly a disease of older people, with about 65% of
deaths at age 65 and older [8]. This ERQCC paper focuses on
There has been a growing emphasis on improving quality in cancer the two main
organisations given variations in outcomes in Europe. The European
Cancer Concord (ECC), a partnership of patients, advocates and
cancer professionals, recognised major disparities in the quality of
cancer management and in the degree of funding in Europe. Its
European
Cancer Patient’s Bill of Rights is a patient charter that underpins equi-
table access to optimal cancer control, cancer care and research for
Europe’s citizens [1].
This followed an assessment of the quality of cancer care in
Europe as part of the first EU Joint Action on Cancer, the European
Partnership for Action Against Cancer (EPAAC,
http://www.epaac.eu). It reported that there are important variations
in service delivery between and within countries, with
repercussions in quality of care and patient outcomes. Factors
such as waiting times and provision of optimal treatment can
explain about a third of the differences in cancer survival among
countries. Lack of a national cancer plan that promotes clinical
guide- lines, professional training and quality control measures,
may be responsible for a quarter of the survival differences.
The EU Joint Action on Cancer Control (CANCON), which replaced
EPAAC from 2014, also focused on quality of cancer care and in 2017
published the European Guide on Quality Improvement in
Comprehensive Cancer Control [2]. This recognised that many people
with cancer are treated in general hospitals and not in
comprehensive cancer centres
(CCCs), and explored a model of ‘comprehensive cancer care
networks’ that can integrate expertise under a single governance
structure.
Further, research shows that care provided by multidisciplinary
teams (MDTs) (or multiprofessional teams) results in better clinical
and organisational outcomes for patients [3] and are the core
component in cancer care [4].
Countries have been concentrating expertise for certain tumour
types in such networks and in dedicated centres, or units, such as
those for childhood and rare cancers, and all CCCs have teams for the
main cancer types. However, for common adult tumours, at the
European level there has been widespread effort to establish
universal, dedicated units only for breast cancer, following several
European declarations that set a target at the year 2016 for care of all
patients with breast cancer to be delivered in specialist
multidisciplinary centres. While this target was not met [5], the view of
the ERQCC expert group is that healthcare or- ganisations should
adopt the principles of such dedicated care for all tumour types.

1.1. Lung cancer

Lung cancer is one of the most complex of all common cancers.


The disease is multifaceted, given its complex tumour heterogeneity,
rapidly evolving treatment landscape and huge societal impact. MDTs
are crit- ical to optimal care of patients with lung cancer and have been
discussed and implemented in some countries. It is only recently that a
pan- European survey of organisation has been undertaken, led by the
Eu- ropean Respiratory Society, which revealed important differences
in the infrastructure and delivery of lung cancer care in Europe [6].
This ERQCC paper complements these findings by setting out for a
broad audience the challenges in lung cancer, the essential
requirements for an MDT, and supporting information.

2. Lung cancer: key facts and challenges

2.1. Key facts

2.1.1. Epidemiology

22 2
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
in siblings or parents are at greater risk, although there are currently
no clinical testing options for identified germline variants and no
guidance for medical management of variant carriers [17]. People with
medical conditions such as inflammatory lung disease, tuberculosis,
asthma,

chronic obstructive pulmonary extended with endobronchial


disease (COPD) and pulmonary ultrasound (EBUS) and/or
fibrosis have increased risk [18]. endoscopic ultrasound (EUS)
to evaluate lymph nodes;
2.1.3. Diagnosis and treatment other biopsy procedures
summary include image guided needle
For full diagnosis and biopsy, thoracoscopy and
Fig. 1. European morality and incidence.
Source: European Cancer Information System. New European age stand- treatment detail see European mediastinoscopy. Finally,
ardised rates. Society of Medical Oncology biopsies from a metastatic
(ESMO) guidelines at organ also have to be
https://www.esmo.org/Guid considered.
types of primary lung cancer – non-small cell lung cancer
• (NSCLC) and small cell lung cancer (SCLC). NSCLC is by far the elines/Lung-and-Chest-Tumours, Lung cancers are classified
most common, and National Institute of Health according to the World Health
accounting for about 85% of cases. SCLC is more aggressive and and Care Excellence (NICE) Organi- zation (WHO)
spreads rapidly (metastasises). diagnosis and management histology classification [20].
In 2018, the estimated incidence of lung cancer in European guidance,
• updated March 2019, While NSCLC is staged
Union countries was about 365,000 and mortality nearly at according to the TNM
300,000 [9]. Men https://www.nice.org.uk/ (tumour, node, metastasis)
represent about two-thirds of mortality – nearly 200,000 were pro- g u i d a n c e / n g 1 2 2 [19]. system, SCLC is commonly
jected to die from lung cancer in 2018. There are major grouped into two categories,
• differences Most people do not have, or limited and extensive dis-
among countries: for both sexes, Hungary, Poland, Denmark and have only limited, symptoms ease according to the
Greece were estimated to have much higher mortality (new Euro- when the cancer is at an Veterans’ Administration
pean age standardised rate >70 per 100,000) than Sweden and early stage. Symptoms may staging system. TNM
Finland (<40 per 100,000), and female deaths from lung cancer be due to lung infiltration, staging has recently also
were estimated to be highest in Denmark, Hungary and the such as persistent cough, been proposed for SCLC,
Netherlands. See Fig.1 for regional estimates. modified pattern of chronic having a more prognostic
Survival rates for lung cancer in Europe (combining all stages and • cough due to smoking, value than an operational one.
histologies) are low. The EUROCARE-5 study for the years 2000– coughing up mucous and Molecular diagnostics are now
2007 (the most recent pan-European survival study) reported blood, breathlessness and playing a major role in
5 year relative survival for men in the age group 15–44 at 22%, chest infections; other metastatic adenocarcinoma
dropping to 7% at age 75 [10]. Average 5 year survival for symptoms may be related+to NSCLC owing to the
both other organ involve- ment or discovery of actionable
sexes was 13%. There was only limited improvement in survival may be non-specific such as targets for new drugs.
• during the study years. More recent survival data from England tiredness and weight loss. The therapeutic approach
• and The initial investigation for must take into account patient
Wales for the years 2010–11 showed 1 year survival of about 32% suspected lung cancer is choice, functional status
and 5 year survival of about 10% for both sexes [11]; in Belgium in usually a chest x-ray followed (respiratory and cardiac in
the years 2012–2016, 5 year estimated relative survival was by a computed tomography particular) and co- morbidities
considerably better, at about 18% for males and 27% for females (CT) scan. Further in- such as smoking-related
[12]. Age-standardised 5-year net survival was in the range 10– vestigations for staging conditions (cardiovascular dis-
20% in most of the 61 countries included in CONCORD-3 [13]. assessment may include ease, COPD) and other
While lung cancer remains an enormous burden on European • positron emission conditions (including renal
health services, mortality has declined greatly among men; for tomography (PET)/CT, brain failure, hepatic disease,
example, by 50% in men in the UK over 40 years, owing mostly magnetic resonance imaging chronic viral infections,
to a decline in smoking, and in 27 EU countries there was a (MRI) or CT, bone autoimmune disease). Older
linear decrease in the age standardised mortality rate in men scintigraphy, and upper pa- tients must be informed of
from 77/100,000 in 1994 to 57/100,000 in 2012, with the abdomen CT, adapted treatment options and should
proviso that there was considerable variability among countries according to not remain untreated unless
[14]. Conversely, mortality among women rose from the treatment intent through choice; careful
15/100,000 in 1994 to 20.5/100,000 in 2012, partly due to the (curative or palliative) and
the patient’s con- dition. evaluation, integrating
later uptake of smoking by women, with the geriatric assessment in some
The diagnosis needs
male–female ratio gap narrowing from 5.1–2.8 in this period. cases, is needed before any
histology or cytology
Globally, female lung cancer mortality may surpass breast cancer confirmation. treatment. Similarly, patients
mortality by 2030 [15]. There is a variety of biopsy with poor performance status
techniques depending on the should not be de- nied
2.1.2. Risk factors location of the lesions treatment but evaluated
The primary risk factor is smoking. In Europe more than 90% of (central or peripheral) and the based on the therapeutic
cases in men and 80% in women are caused by smoking. Other risk probability of lymph node opportunities by disease
factors are occupational exposure to substances such as asbestos involvement. Biopsy is stage. Apart from
and silica, ionising radiation (radon in the home) [16], second-hand commonly carried out by comorbidities, performance
smoking and air pollution. People with a family history of lung cancer fibreoptic bron- choscopy, status and patient choice,

22 3
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
stage of the disease is the the standard, defining the at-risk
first variable that guides which may have a role in immunotherapy providing population, the CT method,
treatment decisions. non-surgical candidates added value, and and how to deal with false
• Treatment of NSCLC: with tumours up to 3 cm. consolidative loco- positive findings. In addition,
o Stage I and II: Medically fit Adjuvant chemotherapy is regional radiotherapy a organisational aspects and
patients should be offered a standard for completely validated treat- ment cost-effectiveness should be
surgery, with minimally resected stage II disease option; there are as yet no accounted for. It is stressed
invasive lobectomy using where there are no targeted therapy that man- agement of
video-assisted contra-indications. recommendations. detected nodules above
thoracoscopic surgery o Stage III: Patients with o Prophylactic radiotherapy certain sizes should only be
(VATS) preferred to open locally advanced disease to the brain may be carried out in a
thoracotomy for better may be offered offered in patients with multidisciplinary setting that
outcomes and reduced perioperative therapy limited disease has experience in lung
morbidity. (chemotherapy or responding to imaging and managing
Pneumonectomy and chemoradiotherapy) plus chemoradiotherapy, and suspicious findings, which is
sleeve lobectomy should surgery in selected dis- cussed on a case-by- likely to place more pressure
be restricted to selected operable tumours, case basis for metastatic on resources and
cases when lobectomy is whereas chemo- disease. organisation, but also affords
not feasible; radiotherapy, ideally an opportunity to promote
segmentectomy for very delivered concomitantly lung cancer units.
small T1a tumours is when feasible and • Challenges in lung cancer
2.2. Despite lung cancer being a
under investigation. tolerable, is the mainstay care common disease, most
Stereotactic body in the majority of cases. primary care doctors (GPs)
radiotherapy (SBRT) is the When a tumour is not de 2.2.1. Screening and detection only see one or two new
preferred option for novo amenable to local cases a year and any suspi-
patients unfit for or therapy, patients should • The high rate of diagnosis at cious lesion must be referred
declining surgery if tu- be offered induction advanced stages is a major to a lung physician. A study
mours are less than 5 cm chemotherapy before a challenge in lung cancer, in the UK on more than
and not centrally located. If new evaluation for local and in recent years there 20,000 cases identified that
centrally located, SBRT treatment, or treated as has been a growing interest patients who have more
should be discussed for stage IV. Maintenance in screening. In the United visits to GPs before
feasibility and to determine immunotherapy in non- States, the National Lung investigation are likely to die
the most appropriate progressing patients after Cancer Screening earlier [25]; the reasons for
technique. The same concomitant Trial (NLST) [21], so far the diagnostic delay are, though,
holds for local ablative chemoradiotherapy is a world’s largest randomised complex and multifactorial
therapies (radiofrequency new standard of care. controlled [26].
ablation, microwave and o Stage IV: There is now a • trial (RCT) of using low dose Lowering barriers to chest x-
cryotherapy), wide range of systemic CT, led to a change of ray and CT-scan access,
therapy options in recommendations in the US including the ability of
metastatic NSCLC with to screen healthy people at patients to demand one, are
chemotherapy, a certain level of risk. This possible ways forward in
immunotherapy, and the results of other health systems where GPs
combined chemo- RCTs in Europe (including act as gatekeepers. A better
immunotherapy or the NELSON trial) [22, 23] strategy is said to lie in the
targeted drugs in case of have also led an EU expert use of risk prediction tools to
actionable molecular group to recommend that aid GPs, but there is a
alteration (currently ALK, health or- ganisations pressing need to determine
EGFR, ROS1 and BRAF). prepare for screening [24], which tools are the best to
There is also growing albeit with caution about use [27].
interest in offering
additional local ablative GPs and other professionals connection with smoking may
• treatment in such as community also delay visits to health
oligometastatic lung pharmacists also play a vital services [29], and the success
cancer, with the intent to role in prevention but need of anti-smoking campaigns
obtain long-term disease access to smoking cessation may have given people a
control and potentially a services, which need false sense of se- curity as
cure. adequate funding and about half of people with a
Treatment of SCLC: • availability, and to ed- ucation smoking history who present
o Patients with limited about lung cancer. with lung cancer are not
• disease are treated by As men in Europe form a active smokers, and the
concomitant chemo- large majority of patients with number of non-smokers who
radiotherapy or lung cancer, it is important develop lung cancer is
occasionally may be that barriers to their increasing. Awareness
offered surgery. awareness of symptoms and campaigns need to address
o Metastatic SCLC willingness to seek help are all risk factors; symptom
treatment is mainly addressed [28]. For both awareness campaigns are
palliative with sexes, the stigma attached to associated with a shift to
chemotherapy remaining lung cancer owing to its earlier diagnosis [30,31].

22 4

T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
Many patients with lung for all the new targeted drugs
cancer are first diagnosed in for lung cancer may not be and regional differences are pulmonary physicians who
emergency departments. available at initial diagnosis also reported [38]. Detailed specialise in thoracic
These patients have worse and during the course of the assessment of patient oncology, or can additionally
outcomes, which is another disease, and expertise in suitability and informed administer medical therapy
compelling reason to interpreting molecular decision-making with (such as Portugal and
increase awareness and findings and their clinical patients, their family, carers Sweden), which add impor-
detection, but it is a significance is and primary care doctors are tant skills to the MDT, but
challenging issue [32]. Data important [35]. There is a fundamental parts of lung this specialisation is provided
from 11 hospitals in 8 need for more molecular cancer treatment planning. in only a minority of
countries in Europe showed pathologists and specialised • A large majority of patients countries.
that 23.1% of patients with pulmonary pathologists. • with lung cancer are not There can be wide variability
18 eligible for surgery and it is in treatment outcomes
• lung cancer were diag- F-FDG PET/CT allows more
nosed as part of an precise disease staging in essential that among patients. In data from
emergency presentation, lung cancer multidisciplinary care is the UK, the proportion of
with rates among countries and is essential when given equal weight for all patients with lung cancer
ranging from 13.2%–47.7% curative treatment is intended stages of the disease. alive after 1 year in 2013
(surgery, che- • Lung cancer surgery can be varied by 55% down to just
[33].
moradiotherapy) and must be complex, challenging and 12% in the hospitals that
2.2.2. Diagnosis and staging available at all centres but at high risk, and better treated the disease, and
present may not be on-site. outcomes have been shown even when outliers at the top
• Diagnosing and staging lung Other interventions such as by surgeons specialising in and bot- tom are removed
cancer is complex and it is brain MRI and EBUS may thoracic surgery, but the variation was 48% down
essential that experienced also lack availability. currently there is no to 20% [42]. High volume
specialists including designation of this lung cancer units are
radiologists, pulmonologists, 2.2.3. Treatment and outcomes specialism in all European associated with better
pa- thologists and nuclear countries [39], and patients outcomes [43], even when
• medicine specialists Treatment for lung cancer may be operated on by they have a patient mix with
determine results from can be highly complex and cardiothoracic and general more co-morbidities and of
imaging and pathological the current guidelines have surgeons. Similar con- lower socioeconomic status
samples. A successful many options and siderations hold for [44,45]. These centres are
management plan, especially uncertainties owing to various radiotherapy, with likely to perform more
for radical interventions, levels of evidence and rapidly subspecialisation in thoracic surgical resections as a
depends on their input to the evolving therapeutic oncology advocated for percentage of cases, and
MDT. possibilities, particularly in optimal care. In addition, use more minimally invasive
• It can be challenging to medical treatments. access to advanced techniques such as VATS
obtain adequate biopsy Guidelines stress that MDTs radiotherapy technology and and robotic assisted thoracic
samples in lung cancer in are vital to selecting the best techniques such as intensity surgery (RATS) with lower
both quantity and quality. strategies for local and modulated radiotherapy morbidity (see also MDT
The site having the best advanced disease; (IMRT) and SBRT is section 3.2). It has been
chance for a valuable assessment at necessary to provide optimal reported that if all areas of
pathological sample should multidisciplinary meetings care and outcomes. the UK had the same access
be chosen as early as can change the treatment • After a long period with few to surgery as the cancer
possible. Liquid biopsy (tests plan in a significant number systemic therapies for lung network with the highest
on circulating DNA in blood) of cases [36] but discussion cancer (mainly platinum resection rate, over 5000
to test for EGFR mutations is of new cases in such based chemotherapies), deaths from lung cancer
a non-invasive alternative meetings has been reported there has been a rapid would be pre- vented every 3
that could be added to the to be low in some countries introduction of targeted years [46].
conventional pathological [37] • therapies and Excellent post-operative care
evaluation for appropriate immunotherapies in for patients with lung cancer
patient cohorts. advanced NSCLC, posing can be vital for better
• There are challenges in major challenges for medical outcomes, especially in high-
overstaging or understaging oncologists and respi- ratory risk patients, and can involve
lung cancer concerning physicians on optimal intensive care such as for
infiltration of the treatment algorithms and major cardio-respiratory
mediastinum or suspected toxicity management [40]. In compli- cations. It is
distant me- tastases, leading treating locally advanced important that care is
to misclassification and NSCLC, a survey of organised according to pre-
inadequate treatment specialists in Italy has found operative risk [47].
strategy. • variations in management Lung cancer nurse
• Pathological confirmation is that suggests that specialists are promoted in a
crucial in determining the appropriate multidisciplinary number of countries such as
appropriate treatment plan approaches have not been Belgium, the Netherlands
for patients, especially with mandatory [41]. and the UK as key
the advent of targeted • Some countries (such as components of quality care,
therapies and Belgium, France, Germany but contact with such nurses
immunotherapy in NSCLC and the Netherlands) have may be limited or not
[34]. Molecular diagnostics developed positions for available [48]. The presence

22 5
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
of lung cancer nurses may diagnosed with lung cancer inequalities in access to high-
be associated with greater is increasing and so are the quality care, although been shown that older
receipt of treatment, in support needs of this popu- comparisons are hard to patients are less frequently
particular surgery, as lation, which can include make owing to widely varying discussed by MDTs, which
evidenced in the UK [49]. physical and incidence and quality of may result in lower uptake of
neuropsychological symp- registry information. What is radiotherapy [62]. There is a
2.2.4. Support services and toms such as shortness of certain is that as with other pressing need to develop the
survivorship breath, fatigue, short-term cancers, some countries in evidence base for defining
memory loss and anxiety. eastern Europe lack access the role of treatments such
The long-term survival rate Lung cancer is associated • to drugs, radiotherapy and as chemoradiotherapy and
of those who have been with higher disease burden, new diagnostic tech- niques immunotherapy in older
that may be critical to patients, especially
more physical hardship and will require high-quality improving care, as vulnerable and frail
greater symptom distress palliative and supportive documented by ESMO and individuals. Not age, but
than some other cancer care, which may not be ESTRO for medical comorbidity, life expectancy,
types. There is a need for available at all locations. therapies and radiation and patient preferences
survivorship programmes Symptoms caused by the oncology should be decisive factors
dedicated to lung cancer, disease and its treatments [57–59]. In addition, lack of when offering treatment [63].
owing to the complex nature can be profoundly • well-trained professionals Patients with lung cancer
of the disease and particular debilitating and it is in lung may not only living in more
experience of patients. cancer that studies have limit the availability of the socioeconomically deprived
• Patients with lung cancer are been first carried out on the latest therapeutic advances, circumstances may be less
a neglected population for benefits of early intro- but also limit access to the likely to receive treatment,
psychosocial needs duction of palliative care, current standards of care including surgery and
compared with some other finding benefits not just for [60]. chemotherapy [64]. These
• cancers, partly owing to the patients but also for carers Lung cancer is primarily a inequalities may not be
stigma of the disease as and healthcare systems disease of older people, and accounted for by
being self-inflicted through [53]. due to the demographic socioeconomic differences in
• smoking, and they report A review of supportive care transition, this population is stage at presentation or by
increased distress as a in lung cancer considers it increasing. There are differences in healthcare
result. Failure to detect to be a rapidly expanding pronounced challenges in systems.
distress in pa- and multidisciplinary field caring for a population that
tients might serve as with an urgent need to has several co- morbidities 2.2.7. Research
barriers to treatment, develop more effective and in making shared and
decreasing patients’ interventions and focus on • informed treatment The range of research
health-related quality of life, neglected symptoms [54]. A decisions. In older patients, challenges for lung cancer is
increasing healthcare costs, trial in Belgium has shown treatment decisions are wide, extending from risk
and nega- tively impacting that early and systematic more complex because of stratification and methods of
smoking cessation efforts. integration of palliative care the scarcity of data from diagnosis, to new localised
• Surveillance of survivors is is more beneficial for large randomised studies in treatment techniques and
an increasingly important patients with advanced the elderly and the optimal combination of local
concern as numbers rise, but cancer than palliative care heterogeneity of this and systemic treatment
evidence suggests that more consultations offered on population concerning strategies, to individualising
frequent surveillance after demand, even when functional status, medical treatments as more
surgery is not associated psychosocial support has comorbidity and new agents become
with improved survival [50]. already been offered [55]. polypharmacy [61]. In available for advanced
• Hospi- talisations among A Lancet Oncology Belgium, for example, it has disease, and to improving
long-term survivors are Commission has proposed quality of life.
common and occur most the use of standardised care • However, the global level of
often owing to pathways and MDTs to research on lung cancer
cardiovascular, pulmonary promote integration of relative to its huge burden
and gastrointestinal dis- oncology and palliative care lags significantly behind
eases [51]. [56]; ESMO has introduced that of other cancers [65].
• Carers of patients an accreditation pro- gramme • Evidence also suggests
experience rising emotional, called Designated Centres of that treatment at institutions
physical and financial costs Integrated Oncology & Palli- with an interest in clinical
with increasing incidence of ative Care trials [66] and higher clinical
cancer and other life (https://www.esmo.org/Patien trial accrual volume is
limiting ill- nesses, with lung ts/Designated-Centres-of- associated with longer
cancer likely to be a Integrated-Oncology-and- overall survival [67].
significant contributor, Palliative-Care).
including at end of life [52]. 2.2.8. Cancer registration and
2.2.6. Inequalities data availability
2.2.5. Palliative and supportive
• care The variation in outcomes for • Cancer registration practice,
lung cancer in Europe both coverage and quality are
• Currently, a great majority among and within countries highly unequal across
of patients with lung cancer indicates that there may be Europe [68]. Consequently,

22 6
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
basic epidemiological data in pathways that cover the must be offered promptly as rates, and better patient
on incidence, mortality and patient’s journey from their the disease progresses satisfaction and quality of life,
survival are not uniformly point of view rather than that rapidly. particularly important in
• available for all countries. of the healthcare system. With emergency presentation patients with metastatic
Also, only a minority of Pathways must correspond being a major problem in lung disease. Clinicians also
to current na-
cancer registries can cancer, there must be benefit from support for
provide sufficient data for tional and European pathways to ensure patients difficult decisions, education
evidence-based clinical
the calculation of are seen in lung cancer units and review. At a national
practice guidelines on
parameters necessary for as soon as possible. level, MDTs can also feed into
diagnosis, treatment and
• the assessment of After a diagnosis, it must be better databases for audit and
follow-up. The European
outcomes and quality of clear to the patient which research [85]. It is recognised
Pathway Associ- ation
care [69]. professional is responsible that there are significant
defines a care pathway as
• In a 2015 survey, only 6 for each step in the obstacles to MDTs in cost and
countries – Denmark, “a complex intervention for
treatment pathway and who time, attendance at meetings,
Germany, Hungary, the the
is following the patient team working and leadership,
Netherlands, Slovenia, and mutual decision making and
United Kingdom – reported organisation of care during the journey (usually and potential delays [85].
a lung cancer data processes for a well-defined called a case manager or Lung cancer MDTs were
collection, or audit, group of patients during a patient navigator) [82]. In initially put in place mainly in
programme in addition to a well-defined period”. This some countries, case man- the United States and United
cancer agers during the main Kingdom [85] and are now
broad definition covers
registry [70,71]. The terms such as clinical, stages of treatment are found in a number of hospitals
creation of a pan-European critical, integrated, cancer nurses. in most countries in Europe,
• dataset is a signif- icant patient pathways that are Follow-up, support and care although the proportions of
challenge but will expose also often used. See for long-term survivorship, patients discussed at MDT
variation in practice, identify http://e-p-a.org/care- and pallia- tive care, must be meetings and clinicians who
best practices, show where pathways and also the WHO part of a care pathway. make up the MDT vary
improvement is needed, framework on integrated considerably. Some countries
and guide investment in people- centred health 3.2. Lung cancer units/centres such as Belgium have pro-
resources. In 2018, the services, and MDTs vided financial resources for
European Respiratory http://www.who.int/servicede MDT meetings. A number of
• Society announced its liverysaf ety/areas/people- The diagnosis and treatment studies have shown the
intention to develop centred-care. of lung cancer must be impact of lung cancer MDTs:
harmonised standards for Examples of lung cancer • managed by a core and o Investigators in Australia
lung cancer registration and care pathways are from the extended MDT of compared clinicians’
services in Europe [72]. National Insti- tute for Health professionals described management plans before
and Care Excellence (NICE) below, at a lung cancer unit MDT meetings with the
3. Organisation of care consensus plans post-
[73], the UK NHS Lung or centre. The ERQCC expert meeting [36].
Cancer Clinical Expert group group considers that optimal Of the 55 eligible cases, the MDT
3.1. Care pathways and [74], NHS Cancer care is delivered when all meeting changed management
timelines Programme [75], Cancer members of the core MDT
Council Victoria, Australia work in a single unit or
• Care for people with lung [76], and Cancer Care centre, but it is recognised
cancer must be organised Ontario that some members of the
MDT may be based at nearby
[77]. Integrated care plans procedures and results, with or other locations, which may
(ICPs) have been proposed other delays caused by have part of the expertise
as a way to improve patient- waiting for multiple specialist necessary (such as diagnosis
oriented quality in the highly consultations, lack of rapid and radiotherapy) and
complex diagnosis and MDT assessment, and collaborative structures must
treatment care pathways for surgical and radiotherapy be in place. Some patients
lung cancer [78,79]. ICPs are treatment delays [80]. will not live near specialist
described as structured However, there have been units, in which case there
multidisciplinary care plans mixed results on whether not must be a structure in place
for a specific clinical meeting guideline times has to enable discussion of
condition. They describe the an impact on survival [80]. A patient management in
tasks to be carried out recent study at a single teleconferences with an
together with their timing and centre found that delays in expert centre.
• sequence and the discipline investigation and treatment Lung cancer is one of the few
involved in completing the do not appear to nega- tively cancers for which systematic
task. affect clinical outcomes, but reviews of multidisciplinary
• Delays in referral to a added that studies are management have been
hospital cancer centre from needed to evaluate whether published [83,84], but there
primary care have been efficient work-up and was a lack of evidence of a
addressed above (section treatment influence other causative effect on
2.2.1). The biggest cause of important variables, such as outcomes. Benefits for
delay in secondary care has quality of life, cost of care patients of MDTs include
been reported as access to and access to therapies concordance with guidelines,
definite diagnostic [81].Treatment for SCLC an increase of treatment

22 7
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
plans in 58%. These carry out at least 150 objective of balancing the disciplines:
changes included resections a year, based on recommendations of clinical
additional investigations evidence developed in the guidelines with the needs of the • Pulmonology/respiratory
(59%), changes in country, and that no unit individual lung cancer patient. medicine
treatment modality (19%), should provide a lung To properly treat lung • Pathology
treatment intent (9%), cancer surgical service on cancer, it is essential that the • Radiology
histology (6%) and fewer than 70 patients a core MDT comprises health • Nuclear medicine
tumour stage (6%) year [46]. How- professionals from the following • Thoracic surgery
o Also in Australia, a ever smaller countries have • Radiation oncology
cohort study of set lower targets – the
presentations at MDT Netherlands specifies that • Medical oncology
at least 50 new cases per • Nursing. • Palliative care.
meetings found an
year are treated at each
association with survival hospital that treats lung According to the case, some Some lung cancer centres
[86] cancer, and at least 20 lung
o Although there is a or all of this core MDT meets have two MDTs – one for
resections are carried out to discuss:
substantial gap between diagnostic work-
[91].
actual and optimal up, and a main MDT for
• Audits carried out in • All cases after diagnosis and
evidence-based uptake of treatment. In the UK, for
countries such as Germany staging to decide on optimal
radiotherapy for lung and example, some centres have a
and the UK have now added treatment strategy
other cancers in diagnostic MDT that typically
• metrics on treatment of Patients with a recurrence, or
Belgium, MDT comprises a coordinator or
advanced stages as well as where changes to treatment
recommendations are specialist nurse, a respiratory
the more commonly pro- grammes are indicated
well applied, suggesting physician and a thoracic
collected data on surgical and have multidisciplinary
that there are other radiologist to plan diagnostic
treatment of early stage relevance and/or planned
barriers to optimal work-up, and may include non-
disease and on the quality of deviations from clinical
treatment [62] cancer cases.
lung cancer surgery. The practice guidelines.
o In Italy, a study found See Fig. 2 for a schematic of
inclusion of extended team the lung cancer MDT.
that the implementation members, such as geriatric Healthcare professionals from
of an MDT increased the oncologists and palliative the following disciplines must
1-year survival rate of 3.4. Disciplines in the core MDT
care [55], may also likely to also be available whenever their
patients who underwent expertise is required (the
be playing a key role in
a surgical resection for General statements
outcomes. ‘extended’ MDT):
NSCLC [87] On the basis of the evidence •
o In England, it has been for lung units/centres and • Anaesthesia/intensive care
• The ERQCC expert group
found that geographic recognises that specialists
MDTs, the ERQCC expert • Interventional radiology
variations in treat- ment may have mul- tiple skills
group considers that given • Oncology pharmacy
and survival of patients and certifications and job
current variability of health • Geriatric oncology
were more likely to titles may not convey this.
systems in Europe it is not • Psycho-oncology
reflect differ- ences in The core and extended
possible to define an • Rehabilitation
clinical management MDTs are described as
essential requirement for
between local MDTs specialist areas within which
case volume at a centre in
[45] personnel must have certain
addition to the presence of
o A study in the US skills and knowledge.
the core and extended MDT
suggested improved members described below, • Core MDT members must
survival with an MDT have excellent
but the cor- rect direction is
model versus traditional communications skills to
towards higher volume and
care [88]. engage patients and their
consolidation of treat- ment
Certain countries have centres. • family and carers in the
taken steps in recent years benefits and risks of
to consolidate expertise in therapies to ensure that
3.3. The MDT for lung cancer
high volume lung cancer treatment options are
centres, notably Denmark, explained to, and
Treatment strategies for all
which now carries out
patients with lung cancer must
surgery in just 4 centres,
be decided on, planned and
and also has fewer
delivered as a result of
locations where lung cancer
consensus among a core MDT
is diagnosed and evaluated,
that comprises the most
reduced to 13 sites from
appropriate members for the
about 50 previously [42,89].
particular diagnosis and stage
Some larger countries have
of cancer, and patient
set high targets for lung
characteristics and prefer-
cancer volume. In
ences, with input from an
Germany, the target for a
extended community of
certified lung cancer centre
professionals. The heart of this
is 200 cases a year (all new
decision-making process is
pre- sentations of lung
normally a weekly or more
cancer) [90]. In England,
frequent MDT meeting where all
the target is for all units to
cases are discussed with the

22 8
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239 n
c
e
r

c
e
n
t
r
e
.

are appropriate for, the Essential requirements:


patient, and are not unduly pulmonology/respiratory
influenced by age but more medicine
by medical fitness and
• choice. Pulmonologists must take part
• in all pathways of lung cancer
3.4.1. Pulmonology/respiratory care. Pulmonologists must be
medicine able to interpret all relevant
Pulmonologists, also known imaging studies, including
as chest or respiratory PET/CT and thoracic
physicians, specialise in the ultrasound.
• diagnosis and treatment of all Pulmonologists must be
lung diseases. They are involved experienced in bronchoscopic
in the care of high-risk patients techniques, both diagnostic
such as smokers, patients with (including EBUS) and
chronic bronchitis, COPD or palliative.
• interstitial lung disease and can Those administering medical
prompt these patients to undergo therapy must also meet the
testing for early diagnosis of lung re- quirements of medical
cancer, and play a fundamental oncologists (section 3.4.7).
role in the investigation and
management of patients with 3.4.2. Pathology
suspected or proven lung cancer Pathology, including
[92]. molecular pathology, has a
They are pivotal in the crucial role in lung cancer –
histological and molecular characterisation of histologic and
confirmation of lung cancer molecular subtype is playing an
diagnosis and in mediastinal increasingly pivotal role in the
staging through bronchoscopy MDT for both diagnosis and
and EBUS/EUS. They also have management.
a key role in the assessment of The current WHO
lung function and fitness for histopathological classification
treatment, including surgery and of lung cancer [93] highlights a
radiotherapy. greater use of
F immunohistochemistry for precise
i Pulmonologists are also
involved in the follow-up and character- isation and
g
. management of pulmonary standardised criteria and
comorbidities and side-effects: terminology for diagnosis. This
2 breathlessness, cough, should be performed not only
. haemoptysis, respiratory failure, on resected samples but also
pulmonary infections and on small bi- opsies and
S pneumo- nitis. They are also cytology, given that the majority
c of patients with lung cancer
h involved in palliative care, and,
e again though bronchoscopy, can present with high-stage disease
m help debulk central tumours or and are not surgical candidates
a
insert stents. [94,95]. The WHO classification
t and recent international
i In countries such as
c Germany, Belgium and the statements provide guidance for
Netherlands, pul- monologists molecular testing on carcinoma
o have an option to train as types, especially adeno-
f pneumo-oncologists (called carcinomas, recognising the
thoracic oncologists in the therapeutic importance of
l Netherlands) and are approved targetable ge-
u netic alterations [96].
n to deliver medical therapy to
g patients with lung cancer, and The role of specialist
are also often the lead clinician pathologists includes carrying out
c in the lung cancer MDT. a detailed morphological study of
a the tumour to provide the most

22 9
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
accurate possible diagnosis in • or the mediastinum and to Radiologists must have a
association with theranostic on tumour grading/staging. further investigate profound knowledge of the
biomarkers. Pathologists also They must supply a diagnosis suspected distant TNM lung cancer staging
coordinate molecular testing, including metastases (i.e. to system and its pitfalls
with attention to all pre-analytic appropriate reporting of characterise adrenal [100,101].
biomarker testing results as
proced- ures to preserve tissue • masses or liver lesions). Radiologists must be familiar
recommended by
quality and quantity and to professional organisations – with the strength and
select the most appropriate Radiologists use the limitations of bronchoscopic
International Association for
tumour block/samples. Tissue the Study of Lung Cancer combination of imaging interventions.
management and turnaround (IASLC), European •
modalities to detect tumour Radiologists must be familiar
time for histology and predictive Respiratory Society (ERS), characteristics, determine the with image guided biopsies
biomarkers are particular College of American radiologic disease stage, and radiological treatment
interdisci- plinary challenges for Pathologists (CAP), identify lesions that warrant options (i.e. radiofrequency
the MDT. Association for Molecular tissue sampling for diagnosis ablation, stenting).
Pathology (AMP). • staging, assist in planning
and Radiologists must be familiar
Essential requirements: Pathologists must work in surgical
• or radiation therapy, with treatment responses to
pathology the MDT to favour the best and restage disease extent radio- therapy,
tissue pro- curement after therapy. chemotherapy, targeted
• Pathologists must have procedure and thus improve therapy and immunotherapy,
expertise in lung disease, mainly the success rate of sampling Essential requirements: and adverse events following
in an oncology setting, with and the quality of testing. radiology treatment.
knowledge of current guidelines As immunohistochemistry is • Radiologists must be familiar
and reviews now largely used in the • Radiologists must be with surgical procedures to
diagnosis and investigation familiar with management assist sur- geons in the
of several biomarkers, care guidelines of pul- monary planning of surgery.
must be taken to ensure • nodules [98,99]. State-of-the-art CT, MR
high-quality staining and • Radiologists must know the imaging and PET/CT must
participation in a quality peculiar pattern of lymphatic be available. Radiologists
assurance pro- gramme is and he- matogenous spread must know when to refer a
essential, such as that of lung cancer (including patient to nuclear medicine
promoted by the European uncommon sites of spread). for PET/CT.
Society of Pathology (ESP
Lung External Quality 3.4.4. Nuclear medicine NSCLC: ESMO
Assessment Scheme; Nuclear medicine plays an guidelines state that all
accredited by BELAC, important role in the patients planned for definitive
Belgium’s accreditation management of lung cancer; stage III NSCLC treatment
[102–106] there is evidence of should undergo a diagnostic
body, conforming to ISO
18
17043). the efficacy of F-FDG thin section CT fol- lowed by
With the increasing PET/CT
• in selected clinical 18
F-FDG PET/CT with a CT
importance of molecular indications. technique with adequately
data in therapeutic high
• decisions, access to an Initial staging of patients with resolution for initial staging to
stage I–II NSCLC: For
accredited molecular patients with resectable rule out detectable extra-
pathology laboratory must NSCLC, 18F-FDG PET/CT thoracic extra-cranial
be guaranteed if not on-site. provides more precise metastasis and to assess
disease
potential mediastinal lymph
staging, especially regarding
3.4.3. Radiology node involvement, ideally
the mediastinum, and is
Radiologists are involved in within 4 weeks before the
essential when curative
the early detection, diagnosis, treatment is intended start of treat- ment. Single
staging and restaging of lung (surgery, SBRT). All patients PET-positive distant lesions
cancer and play critical roles in should undergo a diagnostic need pathological confir-
the MDT. Diag- nosis and thin section CT followed by a mation [105,107].
• staging of lung cancer require a 18
F-FDG PET or NSCLC treatment: PET/CT is
broad variety of imaging 18
F-FDG PET/CT with a CT recommended to guide target
modalities [97]: technique with adequately volume delineation in
high resolu- preparation for curative-intent
The initial imaging modality • tion for initial staging to rule radiotherapy or che-
used to evaluate patients out detectable extra-thoracic moradiotherapy in patients
with a sus- pected lung extra- cranial metastasis and with NSCLC; a diagnostic CT
cancer is usually a CT of the to assess potential scan with
chest, which is frequently mediastinal lymph node intravenous iodine contrast
complemented by a PET/CT involvement, ideally within 4 (unless contra-indicated) and
to stage the mediastinum or weeks before the start of diagnostic whole body 18F-
to detect/ exclude distant treatment. Single PET- FDG PET/CT are considered
metastases positive distant lesions need mandatory. The 18F- FDG
MRI is performed to detect • pathological confirmation PET/CT should be performed
brain metastases, to [102–105]. within 3 weeks before start
• investigate a sus- pected Initial staging of patients of
18
infiltration of the chest wall with locally advanced treatment since F-FDG
22 1
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
PET/CT information may • of patients to ensure Outcomes of patients
otherwise be Nuclear medicine maintenance of expertise. undergoing lung cancer
outdated with increasing time departments must be able to • Perioperative care for surgery must be audited
to treatment [108]. Apart perform daily veri- fication patients undergoing lung [117].
from these ESTRO protocols and to react cancer surgery must be
guidelines, EORTC similarly accordingly. Quality- provided by specialist teams 3.4.6. Radiation oncology
recommends FDG/PET in assurance pro- tocols must of nurses (both in the Radiotherapy has a central
the be in place. An option for • operating theatre and on the role in the multidisciplinary
process of target volume ensuring the high quality of wards) and treatment of lung cancer.
definition [109]. In patients PET/CT scanners is • anaesthetists/intensivists
treated with radiotherapy or provided by the European with access to intensive care • In locally advanced NSCLC,
chemoradiotherapy, an initial Association of Nuclear and high dependency beds, which represents the majority
18
F-FDG PET/CT and during Medicine (EANM) through and in a thoracic sur- gical of patients with non-
metastatic lung cancer, it is
follow-up (where suspicion of EARL accreditation. ward also attended by
the treatment of choice – in
relapse cannot be defined physiotherapists and
with all cases with optional
3.4.5. Thoracic surgery paramedical staff. Patients combination with
CT only) are useful for Surgery is carried out on a with early stage lung cancer chemotherapy – for patients
predicting areas with minority of patients with lung must be offered minimally
greater potential for who are inoperable due to
cancer according to a range of invasive surgery where local tumour extent and/or
recurrence or treatment criteria including resectability, medical
appropriate.
failure [105]. inoperability.
cardiorespiratory function and
• SCLC: 18F-FDG PET/CT is
patient fitness and co- • SBRT [111] For patients amenable to
optional in localised disease. morbidities. Traditionally, lung • Guiding biopsies 18
F- surgery, the combination of
PET findings, which modify resection has been performed with the information FDG
radiotherapy and
treatment decisions, should by thoracotomy. Over the past supplied by PET/C chemotherapy has been shown
be pathologically confirmed 15 years there has been an T, to result in similar survival as a
[110]. increase in minimally invasive improving the probability of a surgical multimodality
• Restaging: (a) restaging for surgery, mainly VATS and more successful extraction of treatment [118,119].
detection of local recurrence; recently RATS. Results from a • diagnostic tissue. For patients with early-stage
(b) restaging after initial number of studies demonstrate NSCLC, SBRT is the
treatment (surgery, superior short-term and long- The role of the nuclear reference treatment for
chemoradiotherapy or term outcomes with VATS [112] medicine physician is to inoperable patients or those
radiotherapy); and (c) and RATS [113]. oversee all aspects of PET/CT refusing surgery [120].
restaging for detection of Studies have shown short- • radionuclide therapy for
and In limited disease SCLC,
metastases [103, 104]. term and long-term benefits in patients who require these pro- standard treatment again
managing oncological thoracic cedures, including indications, relies on a com- bination of
Other clinical situations with
procedures by specialised multidisciplinary algorithms chemotherapy and
limited evidence, but with
thoracic surgeons vs non- and man- agement protocols. radiotherapy [121].
ongoing research and promising
specialists [114,115]. There is • In all situations where
preliminary results are:
evidence to suggest that the Essential requirements: radiotherapy is combined
appointment of surgeons with a nuclear medicine with chemotherapy, a
• Evaluating candidates with
full-time thoracic job plan in concurrent administration of
probable oligometastatic
• disease before preference to mixed-practice PET/CT must be available both yields superior
cardiothoracic surgeons is and nuclear medicine outcome, and, more
associated with an overall physicians with expertise in specifically for SCLC, more
increase in lung cancer survival PET/CT must be available. intense schemes (i.e. with
in England [44,116]. early start of radiotherapy,
Lung cancer surgery twice daily radiotherapy
requires certain perioperative delivery) have been shown
facilities and experienced team important for outcome [122].
members to work with surgeons • In NSCLC, recent evidence
on achieving high quality does not support dose
outcomes. escalation beyond
60–66 Gy total dose, but has
Essential requirements: shown that the use of IMRT
thoracic surgery reduces treatment-related
toxicity [123]. Standard
fractionation schedules
Lung cancer surgery must •
be carried out only in
specialist centres by teams
of appropriately trained
surgeons.
There must be at least 2 •
experienced surgeons per
unit who dedicate a
significant amount of their
time to lung cancer. Centres
must have sufficient volume

22 1
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239

are used in case of concurrent chemoradiotherapy, whereas hypo- • In unresectable locally advanced NSCLC, the addition of chemo-
fractionation is advocated for patients who do not receive therapy to radiotherapy improves cure rate in comparison to radio-
concurrent schemes [124]. therapy alone [130].
• In the metastatic setting, besides the typical palliative indications • In metastatic NSCLC, three therapeutic options are currently avail-
such as pain control or the treatment of brain metastases, thoracic able: targeted therapies in case of oncogenic driver mutation
radiotherapy is used to alleviate symptoms related to local tumour (EGFR, ALK, ROS1, BRAF V600E) which demonstrated major
burden (e.g. dyspnoea, cough, vena cava superior syndrome) or as clinical benefit in terms of response rate and progression-free
a consolidation after chemotherapy in the case of SCLC [125]. In survival; chemo- therapy in case of first-line or salvage therapy;
addition, prophylactic radiotherapy is used in SCLC to decrease the and immunotherapy. Immunotherapy has revolutionised the
risk of developing clinically relevant brain metastases [125]. therapeutic approach of wild type NSCLC either administered alone
• An emerging field of interest is using local consolidative treatment or in combination with chemotherapy.
after systemic therapy in patients with oligometastatic disease [126, • In SCLC, chemotherapy has a major role combined with
127]. radiotherapy in limited disease or alone for extensive/metastatic
disease. Currently, immunotherapy has showed promising results
The role of radiation oncologists (or clinical oncologists in some and is considered a standard of care if available, in addition to
countries) is to define the radiotherapy indication in the context of the platinum- etoposide in extensive/metastatic SCLC [131].
MDT and determine the dose-fractionation prescription in keeping with
national and international guidelines. They oversee the radiotherapy Medical oncologists often coordinate the MDT (and the MDT
care pathway from the start with image acquisition in treatment posi- meeting), and they are essential in interpreting the work-up to define
tion, to definition of the target volume and organs at risk, evaluation of the therapeutic strategy and patient selection for a surgical or non-
the treatment plan, and quality of the treatment delivery including surgical approach in coordination with the surgeon and the radiation
image-guidance, motion management and the potential need for adap- oncologist. In coordination with pneumologists, they also interpret
tive radiotherapy, and follow-up. cardiorespira- tory functional assessment and diagnosis/staging in
minimally invasive procedures (bronchoscopy, EBUS/EUS).
Essential requirements: radiation oncology
Essential requirements: medical oncology
• Radiation oncology departments treating lung cancer must have
access to up-to-date radiotherapy technology and techniques such • Access to medical treatment (chemotherapy, immunotherapy, tar-
as IMRT and SBRT, ideally on-site or at a centre through a formal geted therapy) must be provided in a centre or in a specific unit
collaborative agreement that includes a common MDT. dedicated to medical cancer treatment and by specialised
• Radiation oncologists must know the indications of radiotherapy for personnel (medical oncologists and/or pneumo-oncologists). The
lung cancer, and the place, expected efficacy and potential side- centre must have regularly updated protocols for systemic cancer
effects of thoracic radiotherapy in multidisciplinary treatment regi- treatment administration based on international guidelines.
mens. They must have a special interest and expertise in the multi- • Medical oncologists must know the indications of medical treatment
disciplinary treatment of lung cancer and of other thoracic and combined modality protocols (with radiotherapy or surgery) for
malignancies to select the optimal treatment for each patient, lung cancer, as well as the place, expected efficacy and potential
considering the specific oncologic situation and comorbidities. side- effects of each treatment and their combination in
• Multimodal imaging including a CT in treatment position and/or a multidisciplinary treatment regimens.
PET/CT scan are mandatory to define the target volume, along with • Medical oncologists must be aware of clinical trials and their meth-
pathological information obtained through mediastinal staging – odology and conduct performed at their centre or in associated
either EUS-EBUS or mediastinoscopy – in the case of locally centres.
advanced disease. • Medical oncologists must have access to supportive and palliative
• Radiation oncologists treating lung cancer must have a team of ra- care specialists (such as internal medicine specialist, geriatrician,
diation therapists, dosimetrists and medical physicists with endo- crinologist, cardiologist, pneumologist, infectious disease
expertise in lung cancer and thoracic malignancies. specialist, cancer nurse) with interest in lung cancer and thoracic
• Radiation oncologists must be aware of ongoing clinical trials and malignancies and with knowledge of specific adverse events in
their methodology performed at their centre or in associated chemotherapy, targeted therapies and immunotherapy. Liaison with
• centres. The radiation oncology centre must have regularly geriatricians and others with specialist knowledge of older patients
updated protocols for radiotherapy and concurrent must be considered to assess and deliver optimal treatment and
chemoradiotherapy for lung cancer based on international supportive/ palliative care to meet the complex needs of this
guidelines. population.
• Image guidance, motion management and adaptive radiotherapy pol- • Medical oncologists must be responsible for follow-up, including
icies and quality assurance guidelines must be clearly described and management of early and late toxicity, and survivorship issues. Pro-
documented. External quality assurance audits are highly tocols for the management of immune toxicities are recommended.
• recommended. Radiation oncologists must follow up patients to act
on early or late toxicity, and in case of relapse. 3.4.8. Nursing
Nurses provide information, care and support to patients and their
3.4.7. Medical oncology families throughout the patient pathway. They are a key contact for pa-
tients, provide information to facilitate informed decision-making for
• Medical treatments are essential for therapeutic management of treatment options, advocate for patients’ wishes and concerns in the
both NSCLC and SCLC, whatever the disease extent. MDT, undertake holistic needs assessment, and help manage
• Adjuvant platinum-based chemotherapy has increased survival in symptoms. Due to
the increasing complexity of care, specialised cancer nursing carried
early stage (IB–IIIA) completely resected NSCLC [128] while in-
duction chemotherapy has also proved effective [129]. out by advanced nurse practitioners is in place in some countries and
• In borderline resectable IIIA disease, chemotherapy is always part the skill set they bring is being recognised internationally [48]. In lung
of the multimodality treatment approach, whichever local treatment cancer, recent research suggests that their specialist knowledge can
strategy – surgery or radiotherapy – is considered [118,119]. result in better outcomes in terms of life expectancy, avoiding

230
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
unnecessary hos- pital admissions and managing the effects of
treatment [132].

230
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
death.
Introducing advanced practice nurses can pose organisational
chal- lenges regarding acceptance of the role from the perspective of
patients and healthcare professionals. This was explored in a study
from Switzerland [133] and application of a framework developed in
the Ca- nadian healthcare system [134]. In contrast, such roles have
been in place in other countries for some time; for example, the
National Lung Cancer Forum for Nurses in the UK was established in
1999 to provide networking and support to nurses specialising in the
care of people with lung cancer (https://www.nlcfn.org.uk). The
Netherlands has a similar pulmonary oncology network for nurses
and nurse specialists that aims to optimise care
(http://www.oncologieverpleging.nl/45/pulmonale-oncologie).
The ERQCC group recognises also the contribution of the
European Oncology Nursing Society (EONS) and its Recognising
European Cancer Nursing (RECaN) project
(https://www.cancernurse.eu/research/re can.html).

Essential requirements: nursing

• Nurses must conduct holistic nursing assessments to ensure safe,


personalised and age-appropriate nursing care, and promote self-
efficacy throughout the patient journey. They must promote a cul-
ture of shared decision-making.
• Nurses must provide information and education to both the patient
and family, provide signposting to support organisations, and be
the point of contact where they act as case managers.
• Nurses must ensure systematic screening throughout the disease
trajectory to uncover physical symptoms such as pain and
dyspnoea, psychosocial distress, impairment of physical
functioning, malnu- trition and frailty. Validated instruments (e.g.
distress thermometer) must be used where appropriate.
• Healthcare systems must consider implementing roles for
specialist/ advanced lung cancer nurse practitioners as part of the
MDT.

3.5. Disciplines in the extended MDT

3.5.1. Anaesthesia/intensive care


Anaesthesiologists have key roles in the management of patients
undergoing surgery for lung cancer. These include:

• Surgical risk assessment


• Preoperative optimisation of co-existing medical conditions
• Perioperative clinical pathway management (including intra-
operative care)
• Postoperative management and management of complications in
intensive/critical care facilities
• Acute and chronic pain management.

Enhanced recovery pathway guidelines for lung cancer surgery


have recently been published and should be implemented to facilitate
peri- operative care [135].
Several risk models are available to predict post-operative
outcomes following lung cancer surgery. Estimation of the risk of death
(such as by Thoracoscore) ensures the patient is aware of the risk
before giving consent for surgery [136].
Surgical centres must have the necessary anaesthetic and critical
care expertise and infrastructure not only to manage elective lung
cancer surgery but also to provide the often complex support for
postoperative complications in high-risk patients, which may include
extended car- diovascular support and invasive ventilator support.

Essential requirements: anaesthesia/intensive care

• Patients undergoing lung cancer surgery must have appropriate


preoperative assessment led by anaesthesiologists, who must use
a global risk score such as Thoracoscore to estimate the risk of

23 1
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
stratification and shared decision-making. This must take into account
Anaesthesiologists undertaking lung cancer surgery must have
adequate experience in thoracic surgery anaesthesia including •
current knowledge – and gaps in specific treatments,
one- lung ventilation, the use of double-lumen endotracheal tubes knowledge – of survival outcomes including in- teractions with
and bronchial blockers, and awake fibre optic bronchoscope other treatments
and
intubation; and epidural analgesia and thoracic regional toxicity in this older population • Counsel patients about their
techniques. drug treatment
given the recent increase in
Postoperative care must be undertaken on a thoracic surgery • • Supervise the preparation of
treatment options such as
ward or in intensive/critical care facilities. oncology drugs.
immunotherapies, and lack of
representation of older patients
3.5.2. Interventional radiology Essential requirements:
in clinical trials [145]. oncology pharmacy
Interventional radiologists must be available whenever their
exper- tise is required for biopsy or treatment [137]. Essential requirements:
• Image-guided percutaneous biopsy has become the modality of Oncology pharmacists must
geriatric oncology
have experience with
choice for diagnosing lung cancer, and in the era of target therapies
is•a tool to help define earlier patient-specific tumour phenotypes for antineoplastic treatments and
All older patients (70 ) must
supportive care; interactions
per- sonalised therapy [138]. be screened with a simple
Interventional radiologists also play a role in palliative between drugs; drug dose
frailty screening tool, such as
adjustments based on age,
situations for patients with thoracic pain or haemoptysis. the adapted Geriatric-8 (G8)
liver and kidney function, and
A further role is in the treatment of patients who are not [146].
toxicity profile; utilisation and
candidates
• for surgery and/or radiation therapy mainly as a result of Frail and disabled patients
monitoring of
cardiorespi- ratory comorbidity or insufficient vital lung function. must undergo a geriatric
Therefore, the role of the interventional radiologist is to: pharmacotherapy; pa- tient
assessment [147]. The
counselling and
assessment can be based on
pharmacovigilance; and
Evaluate clinical risks and nodule imaging characteristics before • self-report combined with
knowledge of com-
performing image-guided percutaneous core needle biopsy of un- objective assessments that
plementary and alternative
clear pulmonary lesions or mediastinal and hilar lymph nodes can be performed by a
medicines.
Provide expertise and support for ablative treatment (which may • specialist nurse in
• also be carried out by radiologists) in selected non-surgical patients Oncology pharmacists must
collaboration with a physician
comply with the European
[139–142] (geriatrician/specialist in
Quality Standard for the
Perform interventional pain management techniques for patients • internal medicine).
Oncology Pharmacy Service
with thoracic chest wall pain who do not have effective pain relief • Cognitive impairment affects
• all aspects of treatment – (QuapoS) [149]. Oncology
with conventional pharmacologic treatment or radiation therapy.
ability to consent, compliance drugs must be prepared in the
These procedures include intercostal nerve blocks/neurolysis,
with treatment, and risk of pharmacy and dispensing
para- vertebral nerve blocks/neurolysis, and radiofrequency
delirium – and screening must take place under the
ablation of thoracic nerves
using tools such as Mini-Cog supervision of the oncology
• Perform embolisation of massive haemoptysis. [148] is essential. A geriatric pharmacist. Oncology
psychiatrist or neurologist pharmacists must provide
Essential requirements: interventional radiology would preferably be involved personalised information for
with impaired patients. patients on their drug therapy
• Image-guided biopsies must be performed by an experienced • For frail and disabled to support adherence.
inter- ventional radiologist with access to appropriate patients, a geriatrician or
• Oncology pharmacists must
interventional CT equipment (CT-fluoroscopy and 3D-CT imaging specialist nurse must be work with medical oncologists
are recommended). Interventional radiologists must be available • present in the MDT meeting on clin- ical lung cancer trials.
to the MDT to discuss the role and proposed use of local ablative to discuss treatment options
techniques for treating lung cancer in patients not amenable to, or aligned with the patient’s 3.5.5. Psycho-
combined with, surgery or radiotherapy.
goals of care. oncology/psychosocial
Interventional radiologists must have access to angiography and • care
expertise in palliative treatments such as embolisation for patients 3.5.4. Oncology pharmacy Many patients with lung
with haemoptysis or pain therapies including intercostal nerve Oncology pharmacy plays a cancer are highly distressed
blocks/neurolysis, paravertebral nerve blocks/neurolysis, and abla- critical role in the extended MDT before, during and after
tion of thoracic nerves. in the care of patients with lung treatment. The overall prevalence
cancer, given the importance of rate of distress for lung cancer
3.5.3. Geriatric oncology systemic treatment. The has been put at about 43% [150],
The MDT must have access to geriatricians with oncology experi- complexity and often low safety and about half of patients were
ence, or specialist geriatric/medical oncologists. Older patients with profile of oncology drugs interested in accessing one or
lung cancer require particular attention to ensure they are not under- together with the high cost of more psychological services
or overtreated; treatment decisions should not be based on drugs involved in lung cancer [151]. Some reports show that in
chronological treatment means that it is newly diagnosed patients the
age but on patient’s health and preference. essential to optimise incidence of depres- sion is even
The role of the geriatric specialist is to coordinate pharmacotherapy. higher, approximately 50%, and
recommendations to other specialists about the need for personalised The role of the oncology about 1 in 3 in patients with
treatment for older patients with increased vulnerability. Performing pharmacist is to: metastatic lung cancer are
geriatric assessment using appropriate tools can help select depressed [152,153].

appropriate treatments with improved outcomes (including quality of Liaise with the medical Depressive coping, emotional
life) and reduced toxicities [143,144]. oncologist/clinical distress, and anxiety have been
The aim must be to provide optimal, personalised care, including oncologist/respiratory found to be associated with
early supportive and palliative care, to older patients through risk physician to discuss cancer shorter survival and increased

23 2
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
lung cancer-specific mortality, • Psychosocial interventions advanced lung cancer [162].
after controlling for might act as a barrier to must be based on clinical Evidence for prehabilitation
demographic, biomedical, and practice guidelines or the – exercise delivered prior to
treatment, decrease patients’
treatment prognosticators [154]. NCCN Guidelines for lung cancer surgery or
health related treatment – is in its early
Failure to detect increased quality of life, increase Distress Management (http
stages but it may have a
levels of distress healthcare costs, and s://www.nccn.org/profession positive impact on the
negatively impact on smoking als/physician_gls/default.asp occurrence and severity of
cessation efforts. x). postoperative complications
Although psychosocial after minimally invasive surgery
3.5.6. Rehabilitation [163].
screening and care is becoming
There is growing evidence Smoking cessation is
increasingly embedded in lung
for exercise interventions to important for all patients with
cancer care [155], health-
reduce morbidity in lung cancer, lung cancer, but cessation
related stigma has not been
to prevent deterioration and to should not be a condition for
fully addressed in supportive
maximise or restore physical offering treatment. A Cochrane
care [156], suggesting that
status prior to, during and review did not find effectiveness
priority should be given to
following treatment [159]. of any type of smoking
interventions that enhance
Pulmonary rehabilitation cessation pro- gramme for
stigma resistance skills and
exercise programmes after people with lung cancer [164],
resilience [157].
surgery or treat- ment aim to but there are no RCTs, and the
At cancer centres, psycho-
restore physical status and to ERQCC expert group considers
oncologists are essential
maximise function, physical that while more research is
members of the extended team
activity, psychological status needed, a service must be in
in addressing such concerns.
and health-related quality of life; place for patients.
Their role is to:
exercise for people with
advanced lung cancer aims to Essential requirements:
Ensure that psychosocial •
prevent deterioration in physical rehabilitation
distress [158], and other
psychological disorders and and psychological status and

maximise independence [159, Physiotherapists trained to
psychosocial needs, are •
160]. Exercise training after provide exercise
identified by screening
NSCLC surgery has been programmes to patients with
throughout the disease
shown to be important in lung cancer after treatment
continuum, and are
postoperative management must be available in the
considered by the MDT
[161]. Larger trials are needed hospital and after discharge.
Promote effective
to confirm and expand • A smoking cessation service
communication between must be available locally for
patients, family members knowledge on the effects of
patients.
and healthcare exercise in patients with
professionals
Support patients and family 3.5.7.
• Palliative care meeting major unmet needs,
members in coping with Palliative care, as defined including in lung cancer, and
multifaceted disease effects. by the World Health ESMO has proposed the use
Organization, applies not only of the term ‘patient-centred care’
Essential requirements: at end of life, but throughout to encompass both supportive
cancer care (http://www.who.int and palliative care [168].
psycho-
oncology/psychosocial care /cancer/palliative/definition). An important study found that,
Palliative care means patient compared with patients receiving
Psychosocial care must be and
• family centred care that standard care, patients with
provided at all stages of the enhances quality of life by metastatic NSCLC receiving
disease and its treatment for preventing and treating early palliative care had less
patients and their partners physical, psychosocial and aggressive care at the end of life
and families. spiritual suffering [165,166]. but longer survival, and
Patients must have • Supportive care is often used significant improvements in both
psychological assessment as an alternative term that quality of life and mood [169]. A
by the healthcare team. This conveys less stigma about recent review has recommended
can be via a self- advanced cancer (and can lead that early institution of palliative
administered tool (such as a to better take-up of in- care should become a standard
distress ther- mometer). terventions) [167], but is most of care for patients with
Scores below a certain level accurately ‘the prevention and advanced NSCLC [170].
must be routinely managed man- Good communication
by the primary care team; agement of the adverse effects techniques are also essential for
of cancer and its treatment’, as early inte- gration of palliative
above that level there must
be further clinical defined by the Multinational care, to promote prognostic
Association for Supportive Care awareness, and intro- duce or
interviewing and screening in Cancer (MASCC,
for anxiety and depression, adapt advance care planning
https://www.mascc.org). In [171].
and referral to the most recent years,
appropriate professional, Palliative care includes
supportive/palliative provi- sion palliative and supportive care
such as a mental health has become increasingly
physician. provided by oncology
integrated and important in professionals in the MDT and
23 3
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
other clinicians who are signposting to support and
responsible for cancer care, and advocacy organisations, to It is also essential that with respiratory
specialised care provided by a help them understand the support and advocacy professionals to influence
multi- disciplinary palliative care process that will be followed organisations are involved in lung health, and includes
team [172,173]. with their treatment from the • improving quality. These cancer in its remit.
point of diagnosis. They must • groups work to: Conclusions on each case
Essential requirements: be supported and o Improve patients’ discussion must be made
palliative care encouraged to engage with knowledge, understanding available to pa- tients and
their health team to ask and empowerment their primary care physician.
including through
• The MDT must offer optimal questions and obtain Advice on seeking second
information in patient
supportive and palliative care feedback on their treatment. friendly language opinions must be supported.
at the earliest opportunity. • o Fight stigma associated Healthcare providers must
• There must be access to a with the disease publish on a website, or
dedicated palliative care unit o Secure access to make available to patients on
with a specialist team that innovative therapies and request, data on centre/unit
provides expert outpatient improve quality of di- performance.
and inpatient care and good agnostics, treatment and
knowledge of cancer disease care 4.2. Performance and quality
and cancer treatments. o Support lung cancer
• The palliative care team research, such as by 4.2.1. Metrics
must include palliative care being involved in the A lung cancer centre must
physicians and specialist better design of clinical develop:
nurses, working with an trials
extended team of social • o Advocate at Performance measurement
workers, psychotherapists, • European and metrics/quality indicators
physiotherapists, national health based on the essential
occupational therapists, di- policy level. requirements in this paper
eticians, pain specialists and Patient groups and on clinical guidelines, in
psycho-oncologists. and information alignment with national
• The palliative care team include: requirements and legislation
must have experience of • o At European level, Lung Operational policies to
taking care of frail older Cancer Europe (LuCE, ensure the full benefits of a
patients and their families. https://www. coordinated clinical pathway
• To ensure the continuity of lungcancereurope.eu) based on published
care at home, the palliative was established in 2013 guidelines
care team must work with • and has a number of Accountability within the
community/primary care advocacy members, most governance processes in
providers. at national level. LuCE individual institutions
• Palliative care specialists • has been suc- cessful in Systems to ensure safe and
and oncologists must aspire raising awareness of lung high-quality patient care and
to meet the standards of cancer challenges at the experience throughout the
ESMO Designated Centres Eu- ropean Parliament clinical pathway
of Integrated Oncology and • and has published reports Effective data management
Palliative Care on challenges and and reporting systems
(http://www.esmo.org/Patient • disparities Engagement with patients,
s/Designated-Centres- of- o The Global Lung Cancer their carers and support
Integrated-Oncology-and- Coalition groups to ensure reporting of
Palliative-Care). (http://www.lungcancerc patient outcomes and
oal ition.org) numbers experience.
4. Other essential several European
requirements advocacy organisations This includes national audits
in its membership and and mandatory participation in
4.1. Patient involvement, has an interactive map some countries (see examples
access to information and detailing statistics in in 4.2.4 below). But as noted,
transparency only 6 countries in Europe have
countries and whether
they have a cancer plan a lung cancer data collection, or
• Patients must be involved in audit, programme (section
and registry, and have
every step of the decision- 2.2.8 above), and the expert
implemented the WHO
making pro- cess. Their group considers there is an
Framework Convention
satisfaction with their care urgent requirement for
on Tobacco Control
must be assessed consistent collection of a
o The European Lung
throughout the patient care minimum set of structure,
Foundation (ELF)
pathway. Patients and their process and outcomes
(http://www.europeanlung.
families and carers must be measures for all centres treating
org), founded by the
offered timely, relevant, lung cancer. Appointing a
European Respiratory
objective and clinical data lead for each MDT
Society (ERS) in 2000,
understandable informa- with allocated time to promote
aims to bring together
tion, which may include data quality is good practice,
patients and the public
decision support aids, and
23 4
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
and ideally a lung cancer All MDT decisions must be specialist follow-up
centre should have a dedicated documented in an • thereafter, which can LCNS present at the time of
data manager as part of the understandable manner, include protocol- led diagnosis, well below targets
MDT. and must become part of clinical nurse specialist of 90% and 80%. The audit
patient records. Decisions follow-up. also included surgery rates in

4.2.2. MDT performance taken The National Lung Cancer NSCLC, which rose to 18.4%,
Audit for England, Wales, and systemic therapy rates in
during MDT meetings must audit examples Guernsey and Jersey for advanced NSCLC and SCLC;
be monitored, and Most national initiatives on the audit year 2017 [179] multimodal treatment rates
deviations reported to the quality in lung cancer care are reported that 37% of were also reported.
MDT. It is essential that all recent, demonstrating that • patients were alive at least As of the end of 2018, the
relevant patient data meet much work needs to be 1 year after diagnosis, a Germany Cancer Society
quality standards and are carried out to embed best significant improvement on reported 52 certified lung
available at the time of the practice, and that variation in the 31% diagnosed in cancer centres. Its annual
MDT meeting. processes is likely to be 2010, but the same as the report detailed surgical case
• The core and extended uncovered. They include the year before; the audit also by tumour stage, stage
MDTs must meet at least following. identified the highest and distribution, and noted that all
once a year to review the lowest-performing regions. centres met the target of
• activity of the previous NICE in the UK has The audit reported on seeing 200 primary cases a
period based on the audited published a quality curative treatment rates for year (median 335.5 cases).
metrics, discuss changes in standard for lung cancer, early stage disease, and There was no target for the
protocols and procedures, updated in March 2019 although the rate was number of lung resections but
and improve the per- [178]; the statements most about 80%, that still left 1 in the median was 106. Most
formance of the unit/centre. relevant to MDT working 5 patients with no curative centres met the target for
MDT performance must be are: treatment. In a change, presenting pretherapeutic
quality assured both o People with known or pathological confirmation cases in an MDT meeting,
internally and by external suspected lung cancer • was reported for early and the rate for presenting
review with demonstration have access to a named stage only, instead of for all recurrent or remote metastatic
of cost-effectiveness of lung cancer clinical patients, as physicians said cases improved. The audit
quality improvements, and nurse specialist who it may not be in the best also records the per- centage
MDT guidance must be they can contact interests of patients with of patients receiving psycho-
promoted nationally and between scheduled advanced disease and oncology care, social services
written into national cancer hospital visits poor status to undergo counselling, and patients
plans. The use of tools and o People with lung cancer invasive biopsy. The rate of participating in clinical
data feedback to improve are offered a holistic patients being seen by a studies, and there are a
MDT performance should needs assessment at lung cancer nurse number of indicators and
be considered [174,175]. each key stage of care specialist (LCNS) did not targets for factors such as the
• The ERQCC expert group that informs their care improve, with 71% of share of pneumonectomies in
strongly recommends that plan and the need for patients being seen and lung resections,
further attention be given to referral to specialist 58% having an bronchoplasty/angioplasty
measures of patient services procedures, revision
reported outcomes, not only o People with lung cancer surgeries, radiotherapy and
to agree which tools should have adequate tissue chemo- radiotherapy,
be used, but also to use samples taken in a pathology and mortality after
them more systematically suitable form to provide surgery (which has a target of
as part of discussions and a complete pathological 5% or less, which all but one
evaluation within the MDT. diagnosis including centre met). Annual reports
For example, symptom tumour typing and and a catalogue of
monitoring via weekly web- subtyping, and analysis requirements for centres are
based patient reported out- of predictive markers available online [90]. A study
comes has been associated o People with lung cancer in Belgium looked at quality
with increased survival are offered assessment and variability of lung cancer
compared with standard for multimodality care in Belgian hospitals.
imaging surveillance in lung treatment by a MDT Twenty indicators were
cancer [176]. comprising all specialist measured for a total of 12,839
core members patients. Good results were
4.2.3. Accreditation o People with lung cancer achieved for 60-day post-
The ERQCC expert group have access to all surgical mortality (3.9%),
strongly recommends appropriate palliative histopathological confirmation
participation in na- tional or interventions delivered of diag- nosis (93%) and for
international accreditation by expert clinicians and the use of PET/CT before
programmes, e.g. Organisation teams treatment with curative intent
of European Cancer Institutes o People with lung cancer (94%). Areas to be improved
(OECI) accreditation, are offered a specialist included the reporting of
http://oeci.selfasse follow-up appointment staging information to the
ssment.nu/cms[177]. within 6 weeks of Belgian Cancer Registry
completing initial (80%), the use of brain
4.2.4. National quality and treatment and regular imaging for clinical stage III

23 5
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
patients eligible for curative radiation oncologists [182] in in advanced studies in lung trials are less available,
treatment (79%), and the time the Dutch Lung Cancer Audit, cancer (htt centres treating lung cancer
between diagnosis and start of which is described as a ps://bit.ly/2OWhmxr). should engage with
• active treatment (median
first unique registry to evaluate An expert group on cancer policymakers to investigate
20 days). High variability the quality of multidisciplinary control at the European referring patients to other
between centres was care [183]. Commission has endorsed a countries (as proposed with
observed for several A practical data set for lung • recommendation for European Reference
indicators. Twenty-three cancer MDT to use for multidisciplinary training of Networks) and should be
indicators were found optimal treatment cancer specialists to improve prepared to participate in
relevant but could not be recommendations and to the value of MDTs and clinical trials from an
measured [180]. Belgium’s evaluate team performance patient care [188]. organisational standpoint.
Health Care has been developed through Researchers at other centres
Knowledge centre (KCE) has a consensus methodology; 6. Clinical research and should be considered as part
also published quality 51 data elements across 8 population registries of the extended MDT for at
indicators for managing lung domains (patient least annual discussion of

cancer [181]. demographics, risk factors, Centres treating lung cancer clinical trial participation.
The Netherlands has set out biopsy data, staging, • must have clinical research Generally, pan-European
standards for hospitals timeliness, treatment, follow- programmes (either their action should be taken to
treating lung cancer, which up and patient selection) ach- own research or as a increase participation of lung
include the MDT set out in this ieved consensus [184]. participant in programmes cancer pa- tients in clinical
paper, and a number of A paper by the lung cancer • led by other centres). The trials (both industry-sponsored
volume requirements. It is a working group of the research portfolio should and academic), and internet
summary of organisational, International Consortium for have both interven- tional access to local clinical trial
technical and clinical Health Outcomes and non-interventional databases should be
requirements [91]. The Measurement (ICHOM) projects and include developed. Older adults are
Netherlands also started the considered that lung cancer academic research. The currently underrepresented in
nationwide Dutch Lung outcome measurement has MDT must assess all new cancer clinical trials despite
Surgery Audit (DLSA) in 2012. been mostly limited to patients for eligibility to take having a disproportionate
Participation in the DLSA is survival, and there is a need part in academic and burden of disease. Strategies
mandatory and required by to include measures of the industry sponsored clinical to increase the participation of
health insurance organi- value of treatments according trials at the centre or in older adults must be
sations and the National to other factors such as research networks. implemented and trials

Healthcare Inspectorate. It is complications, degree of The German Cancer Society designed to take their needs
reported that guideline health, and quality at end of specifies a minimum accrual into account. In lung cancer,
adherence has increased, and life. The authors have put rate for clinical trials of 5% research needed on older
96.5% of lung cancer pa- forward a set of patient- and the OECI requirement for people includes modified
tients were discussed in centred outcomes [185]. CCCs is >10%. The ERQCC schedules of chemotherapy;
preoperative MDTs. Overall The European Organisation • expert group considers that who can best receive
postoperative complications for Research and Treatment the 5% target is an important chemoradiotherapy and
and mortality after NSCLC of Cancer (EORTC) has recommendation for all lung
operations were 15.5% and revised its questionnaire for cancer units.
2%, respectively. The audit assessing quality of life of • Collaboration with European
has been extended to data patients with lung cancer. academic networks is strongly
recom-
from nonsurgical lung cancer The original 13 item
patients, including treatment questionnaire has mended – see the lung
data from pulmonary and cancer group of the EORTC
(http://www. eortc.org), and
the European Clinical
been extended to 29 items, incorporated into specialist Research Infrastructure
primarily to assess treatment postgraduate and Network (ECRIN –
side-effects of traditional and undergraduate curriculums http://www.ecrin.org).
newer therapies [186]. for physicians, nurses and Correlative biomarker
other professionals. research is a crucial part of
5.• Education and training An international curriculum all phases of clinical studies,
in thoracic oncology has and requires close
cooperation with programmes
• It is essential that each lung been devel- oped by the
such as EORTC’s SPECTA
cancer centre provides European Respiratory
(http://www.eortc.org/specta).
professional clinical and Society and the HERMES Prospective monitoring of
scientific education on the (Har- monising Education in lung
disease and that at least one Respiratory Medicine for cancer patient populations
person is responsible for this European Specialists) using real-world data should
programme. Healthcare initiative. It aims to address be carried out through the
professionals working in lung the training needs of mem- use of platforms such as E 2-
cancer must also receive bers of the MDT, any of RADIatE, which is sup-
training in psychosocial whom can lead a thoracic porting radiotherapy
oncology, palliative care, oncology MDT team with research in Europe
rehabilitation and appropriate training [187]. (https://project.eortc.org/e
communication skills. Such The European School of 2-radiate).
• training must also be Oncology offers a certificate In countries where clinical

23 6
T. Berghmans et al. Lung Cancer 150 (2020) 221–
239
immunotherapy in locally 2007: results er_Fact_Sheets_FR_version.
from the EUROCARE-5 study, [13] C. Allemani, T. Matsuda, V. Di
advanced disease, and the References Eur. J. Cancer 51 (15) (2015) Carlo, R. Harewood, M. Matz,
role of immu- notherapy 2242–2253, https://
M. Nikˇsi´c, et al., Global
doi.org/10.1016/j.ejca.2015.07.
generally; and strategies for [1] L. Højgaard, B. Lo¨wenberg, 033.
surveillance of trends in cancer
P. Selby, M. Lawler, I. Banks, survival 2000-14 (CONCORD-
patients aged over 80. K. Law, et al., The European [11] Cancer Research UK;
3): analysis of individual
Cancer control plans must Cancer patient’s Bill of • https://www.cancerresearchuk.o
records for 37,513,025 patients
Rights, update and rg/health-professional/ca ncer-
include high-quality cancer implementation 2016, statistics/statistics-by-cancer-
diagnosed with one of 18
cancers from 322 population-
population and specialist ESMO Open 1 (6) (2017) type/lung-
based registries in 71 countries,
e000127,
registries to inform clinical https://doi.org/10.1136/esmo cancer/survival#heading-Zero.
Lancet 391 (10125) (2018)
open-2016- [12] Belgian Cancer Registry,
research and to improve Cancer Fact Sheet: Lung
1023–1075,
000127.
the quality of care. [2] T. Albreht, R. Kiasuma, M. Van Cancer. ICD10 : C34, 2018. https://doi.org/10.1016/S0140-
6736(17)33326-3.
o A population example is den Bulcke, Cancon Guide – http://kankerregister.org/Canc
[21] National Lung Screening Trial
Nordcan (http://www- Improving Cancer
Research Team, D.R. Aberle, A.M.
Control Coordination, 2017. [14] J.L. Lo´pez-Campos, M. Ruiz-
dep.iarc. fr/NORDCAN), Ramos, E. Fernandez, J.B. Adams, C.
https://cancercontrol.eu/archi D. Berg, W.C. Black, J.D. Clapp,
which includes lung ved/cancercontrol. eu/guide-
Soriano, Recent lung
cancer mortality trends in et al., Reduced lung-cancer
cancer in 50 cancer landing-page/index.html.
Europe: effect of national smoke- mortality with low- dose
types in the Nordic [3] J. Prades, E. Remue, E. van free legislation strengthening, computed tomographic
Hoof, J.M. Borras, Is it worth Eur. J. Cancer Prev. 27 (4) screening, N. Engl. J. Med. 365
countries re-organising cancer services (2018) 296–302, https://doi.org/ (5) (2011) 395–409,
o The Danish Lung Cancer on the basis of 10.1097/CEJ.000000000000035 https://doi.org/10.1056/NEJMoa1
multidisciplinary teams 102873.
Registry (DLCR) has 4.
[22] J.K. Field, S.W. Duffy, D.R.
(MDTs)? A systematic review [15] J.C. Martín-S´anchez, N. Lunet,
recorded all primary lung of the objectives and Baldwin, K.E. Brain, A. Devaraj,
A. Gonz´alez-Marro´n, C. Lido´n-
cancer cases since the organisation of MDTs and their Moyano, N. Matilla- Santander, R. T. Eisen, et al., The UK Lung
Cancer Screening Trial: a pilot
year 2000 and includes impact on patient outcomes, Cl`eries, et al., Projections in
Health Policy (New York) 119 (4) randomised controlled trial of
patient char- acteristics breast and lung cancer mortality
(2015) 464–474, among women: a Bayesian low-dose computed tomography
such as age, sex, https://doi.org/10.1016/j. analysis of 52 countries screening for the early detection
healthpol.2014.09.006. of lung cancer, Health
diagnostic procedures, [4] J.M. Borras, T. Albreht, R. Audisio,
worldwide, Cancer Res. 78
Technol. Assess. 20 (40) (2016)
histology, tumour stage, E. Briers, P. Casali, H. Esperou, et (15) (2018) 4436–4442,
https://doi.org/10.1158/0008- 1–146,
al., Policy
lung function, https://doi.org/10.3310/hta20400.
statement on 5472.CAN-18-0187.
performance, multidisciplinary cancer care, [16] S. Darby, D. Hill, A. Auvinen, J.M.
[23] H.J. de Koning, C.M. van der Aalst,
P.A. de Jong, E.T. Scholten, K.
comorbidities, type of Eur. J. Cancer 50 (3) (2014) Barros-Dios, H. Baysson, F. Nackaerts, M.
475–480, Bochicchio, Radon in homes and
surgery, and/or A. Heuvelmans, et al., Reduced
https://doi.org/10.1016/j.ejca. risk of lung cancer: collaborative lung-cancer mortality with volume
oncological treatment and 2013.11.012. analysis of individual data from 13 CT screening in a randomized
complications. Since [5] F. Cardoso, L. Cataliotti, A. European case-control studies, trial, N. Engl. J. Med. 382 (6)
Costa, S. Knox, L. Marotti, E. BMJ 330 (7485) (2005) 223, (2020) 503–513, https://doi.org/
2013, it also includes
Rutgers, et al., European https://doi.org/ 10.1056/NEJMoa1911793.
patient reported outcome Breast Cancer Conference 10.1136/bmj.38308.477650.63. [24] M. Oudkerk, A. Devaraj, R.
measures [189]. manifesto on breast [17] D.R. Koeller, R. Chec, G.R. Vliegenthart, T. Henzler, H.
Oxnard, Hereditary lung cancer Prosch, C.P. Heussel,
Research based on the centres/units, Eur. J. Cancer
risk: recent discoveries
72 European position statement
data in DLCR has and implications for genetic on lung cancer screening,
(2017) 244–250,
included comorbidity and https://doi.org/10.1016/j.ejca.201
counseling and testing, Curr. Lancet Oncol. 18 (12) (2017)
Genet. Med. Rep. 6 (2) (2018)
inequality 6.10.023. 83–88,
e754–e766,
[6] T.G. Blum, A. Rich, D. Baldwin, P. https://doi.org/10.1016/S1470-
o I–O Optimise is a pan- Beckett, D. De Ruysscher, C. https://doi.org/10.1007/s40142-
2045(17)30861-6.
European research Faivre-Finn, et al., 018-0140-2.
[25] E.L. O’Dowd, T.M. McKeever,
platform based on real The European initiative for [18] L.M. Seijo, J.J. Zulueta,
D.R. Baldwin, S. Anwar, H.A.
world evidence in lung quality management in lung Understanding the links between Powell, J.E. Gibson, et al., What
cancer treatment [190]. cancer care, Eur. Respir. J. 43 lung cancer, COPD, and characteristics of primary care
(5) (2014) 1254–1277, emphysema: a key to more and patients are associated with
effective treatment and early death in patients with lung
https://doi.org/10.1183/090319
7. Conclusion 36.00106913. screening, Oncology 31 (2) cancer in the UK? Thorax 70 (2)
(2015) 161–168,
[7] F. Bray, J. Ferlay, I. (2017) 93–102,
https://doi.org/10.1136/thoraxjnl-
Taken together, the Soerjomataram, R.L. Siegel, http://www.cancernetwork.com/o 2014-205692.
L.A. Torre, A. Jemal, Global ncology-journal/understan [26] L. Walton, R. McNeill, W. Stevens,
information presented in this cancer statistics 2018: ding-links-between-lung- M. Murray, C. Lewis, D. Aitken, et
paper provides a description of GLOBOCAN estimates of cancer-copd-and-emphysema- al., Patient perceptions of barriers
the essential requirements for incidence and mortality key-more-effective-trea tment- to the early diagnosis of lung
worldwide for 36 cancers in and. cancer and advice for health
establishing a high-quality lung 185 countries, CA Cancer J. [19] R. Maconachie, T. Mercer, N. service improvement, Fam. Pract.
cancer service. The ERQCC Clin. 68 (6) (2018) Navani, G. McVeigh, Lung 30 (4) (2013) 436–444,
expert group is aware that it is 394–424, cancer: diagnosis and https://doi.org/
https://doi.org/10.3322/caac.2149 management: summary of 10.1093/fampra/cmt001.
not updated NICE guidance, BMJ [27] M. Schmidt-Hansen, S.
2.
possible to propose a ‘one size [8] J. Didkowska, U. 364 (2019) l1049, Berendse, W. Hamilton, D.R.
fits all’ system for all countries, Wojciechowska, M. Man´czuk, https://doi.org/10.1136/bmj.l104 Baldwin, Lung cancer in
J. Łobaszewski, Lung cancer symptomatic patients
but urges that access to MDTs 9.
epidemiology: contemporary [20] W.D. Travis, E. Brambilla, A.G. presenting in primary care: a
and specialised treatments is and future challenges
Nicholson, Y. Yatabe, J.H.M. systematic review of risk
guaranteed to all worldwide, Ann. Transl. Med.
Austin, M.B. Beasley, et al., The prediction tools, Br. J. Gen. Pract.
people with lung cancer. 4 (8) (2016) 150, 67 (659) (2017) e396–e404,
https://doi.org/10.21037/atm.2016 2015 World Health Organization
classification of lung tumors: https://doi.org/
.03.11.
10.3399/bjgp17X690917.
Declaration of Competing [9] European Cancer Information impact of genetic, clinical and
[28] D.E. Braybrook, K.R. Witty, S.
System (ECIS); radiologic advances since the
Interest https://ecis.jrc.ec.europa.eu. 2004 classification,
Robertson, Men and lung cancer: a
[10] S. Francisci, P. Minicozzi, D. J. Thorac. Oncol. 10 review of the barriers and
Pierannunzio, E. Ardanaz, A. (9) (2015) 1243–1260, facilitators to male engagement in
The authors declare no symptom reporting and screening,
Eberle, T.K. Grimsrud, et al., https://doi.org/10.1097
conflicts of interest for this / J. Mens Health 8 (2) (2011),
Survival patterns in lung and
paper. pleural cancer in Europe 1999-
JTO.00000000000006 https://doi.org/10.1016/j.jomh.2011
30. .03.002.

23 7
T. Berghmans et al. Lung Cancer 150 (2020) 221–
[29] L. Carter-Harris, C.P. Hermann, 10.1136/thoraxjnl-2017- 239
related financial strain at the end
J. Schreiber, M.T. Weaver, S.M. cancer, Asia. J. Clin. Oncol. 12 210710. of life: a cross-national
Rawl, Lung (2) (2016) e298–304, [46] NHS England, Service population-based study, Eur. J.
cancer stigma predicts timing Specifications. Thoracic
https://doi.org/10.1111/ Public Health 24 (5) (2014)
of medical help-seeking Surgery – Adults, 2017.
ajco.12192. 819–826,
behaviour, Oncol. Nurs. https://www.england.N.H.
[37] B.A. Campbell, D. Ball, F. Mornex, S.uk/wp- https://doi.org/10.1093/eurpub/cku
Forum 41 (3) (2014) E203– Multidisciplinary lung cancer content/uploads/2017/07/t 026.
210, meetings: horacic-surg
[53] P. Bhattacharya, S.K. Dessain,
https://doi.org/10.1188/14.ON improving the practice of ery-service-specification.pdf. T.L. Evans, Palliative care in
F.E203-E210. radiation oncology and facing [47] A.P. Meert, B. Grigoriu, M. lung cancer: when to start,
[30] M.P.T. Kennedy, L. Cheyne, M. future challenges, Respirology 20 Licker, P.E. Van Schil, T. Curr. Oncol. Rep. 20 (11)
Darby, P. Plant, R. Milton, J.M. (2) (2015) 192–198, Berghmans, Intensive care in (2018) 90,
Robson, et al., Lung cancer https://doi.org/10.1111/resp.1245 thoracic oncology, Eur. Respir. https://doi.org/10.1007/s11912-
stage-shift following a 9. J. 49 (2017) 1602189, 018- 0731-9.
symptom awareness [38] D. Franceschini, A. Bruni, P. https://doi.org/10.1183/
Borghetti, N. Giaj-Levra, S. [54] A. Molassiotis, W. Uyterlinde, P.J.
campaign, Thorax 73 13993003.02189-2016. Hollen, L. Sarna, P. Palmer, M.
Ramella, L. Buffoni, et al.,
(12) (2018) 1128–1136, [48] I. Stewart, A. Leary, A. Tod, D. Krishnasamy,
Is multidisciplinary management
https://doi.org/10.1136/thoraxjnl- Borthwick, A. Khakwani, R. Supportive care in lung cancer:
possible in the treatment of lung
2018-211842. cancer? A report from three Hubbard, et al., Barriers to milestones over the past 40
[31] L. Ironmonger, E. Ohuma, N. Italian meetings, Radiol. Med. delivering advanced cancer years, J. Thorac. Oncol. 10 (1)
Ormiston-Smith, C. Gildea, C.S. 125 (2) (2020) 214–219, https:// nursing: a workload analysis of (2015) 10–18,
Thomson, M. specialist nurse practice linked https://doi.org/10.1097/JTO.00
doi.org/10.1007/s11547-019-
D. Peake, An evaluation of the 01094-w. to the English National Lung 00000000000407.
impact of large-scale Cancer Audit, Eur. J. Oncol.
[39] G. Massard, M.B. Antonoff, [55] G. Vanbutsele, K. Pardon, S.
interventions to raise public
awareness of a lung cancer J.L. Noel, A. Brunelli, F. Nurs. 36 (2018) 103–111, Van Belle, V. Surmont, M. De
symptom, Br. J. Cancer 112 (1) Farjah, M. Lanuti, et al., https://doi.org/10.1016/j.ejon.201 Laat, R. Colman, et al., Effect of
(2015) 207–216, Transatlantic editorial: 8.07.006. early and systematic integration
https://doi.org/10.1038/bjc.2014. thoracic surgeons need [49] I. Stewart, A. Khakwani, R.B. of palliative care in patients with
596. recognition of competence in Hubbard, P. Beckett, D. advanced cancer: a randomised
[32] Y. Zhou, G.A. Abel, W. Hamilton, thoracic oncology, Eur. J. Borthwick, A. Tod, et al., Are controlled trial, Lancet Oncol. 19
K. Pritchard-Jones, C.P. Gross, Cardiothorac. Surg. 52 (4) (2017) working practices of lung cancer (3) (2018)
611–615, https://
F.M. Walter, et al., Diagnosis of nurse specialists associated 394–404,
doi.org/10.1093/ejcts/ezx294.
cancer as an emergency: a with variation in https://doi.org/10.1016/S1470-
[40] T. Berghmans, M. Evison, T.G.
critical review of current Blum, N. Peled, J. Cadranel, people’s receipt of 2045(18)30060-3.
evidence, New drugs in thoracic oncology: anticancer therapy? [56] S. Kaasa, J.H. Loge, M. Aapro, T.
Nat. Rev. Clin. Oncol. 14 (1) needs and knowledge – an Lung Cancer 123 (2018) Albreht, R. Anderson, E. Bruera, et
(2017) 45–56, 160–165, al.,
online ERS Lung Cancer
https://doi.org/10.1038/ assembly survey, ERJ Open https://doi.org/10.1016/j.l Integration of oncology and
nrclinonc.2016.155. ungcan.2018.07.022. palliative care: a Lancet Oncology
Res. 4 (3) (2018) 00040–
[33] T. Newson-Davis, R. Beradi, N. [50] T.L. McMurry, G.J. Stukenborg,
02018, https://doi.org/10.1183/ Commission, Lancet Oncol. 19
Cassidy, L. Coate, A. L.G. Kessler, G.A. Colditz, M.L.
23120541.00040-2018. (11) (2018) e588–e653,
Wong, A.
Figueiredo, G. Gamerith, et al., [41] A. Bruni, N. Giaj-Levra, P. https://doi.org/10.1016/S1470-
B. Francescatti, et al., More
Emergency diagnosis of lung Ciammella, V. Maragna, K. 2045
frequent surveillance following
cancer: an international Ferrari, V. Bonti, et al., (18)30415-7.
lung cancer resection is not
problem, J. Clin. Oncol. 33 (15) Management of locally [57] N. Cherny, R. Sullivan, J.
associated with improved
(2015), advanced non-small cell lung Torode, M. Saar, A. Eniu, ESMO
survival: a nationally
https://doi.org/10.1200/jco.2015 cancer in the modern era: a European Consortium Study on
representative cohort study,
.33.15_suppl.6536, national Italian survey on the availability, out-of-pocket
Ann. Surg. 268 (4) (2018) 632–
6536–6536. diagnosis, treatment and costs and accessibility of
639, https://doi.org/10.1097/
[34] A. Khakwani, A.L. Rich, L.J. multidisciplinary approach, SLA.0000000000002955. antineoplastic
Tata, H.A. Powell, R.A. Stanley, PLoS One 14 (11) (2019) [51] G.X. Wu, P.H.G. Ituarte, B. medicines in Europe, Ann. Oncol.
D.R. Baldwin, et al., The e0224027, Ferrell, V. Sun, L. 27 (8) (2016) 1423–1443,
pathological confirmation rate of https://doi.org/10.1371/journal. Erhunmwunsee, D.J. Raz, et https://doi.org/
lung cancer in England using pone.0224027. 10.1093/annonc/mdw213.
al., Causes of death and
the NLCA [42] M. Beishon, Ending [58] J.M. Borras, P. Dunscombe, M.
hospitalization in long-term Barton, C. Gasparotto, N. Defourny,
database, Lung Cancer 79 (2) substandard treatment in lung cancer survivors: a
(2013) 125–131, C. Grau, et al.,
lung cancer, Cancer World population-based appraisal, Clin.
https://doi.org/10.1016/j. Assessing the gap between
May/ July (2017). Lung Cancer 21 (3) (2020) 204– evidence based indications for
lungcan.2012.11.005.
https://cancerworld.net/spotli 213, https:// radiotherapy and actual practice
[35] N.A. Brown, D.L. Aisner, G.R. doi.org/10.1016/j.cllc.2019.08.00
ght-on/ending-substandard- in European countries, Value
Oxnard, Precision medicine in 7.
treat ment-in-lung-cancer. Health 18 (7) (2015) A481–
non-small cell lung cancer: [52] L. Pivodic, L. Van den Block, K.
[43] H. Møller, S.P. Riaz, L. A482, https://
current standards in pathology Pardon, G. Miccinesi, T. Vega
Holmberg, E. Jakobsen, J. doi.org/10.1016/j.jval.2015.09.1
and biomarker interpretation, Lagergren, R. Page, et al., High Alonso, N. Boffin, et al., Burden 311.
Am. Soc. lung cancer surgical procedure on family carers and care-
Clin. Oncol. Educ. Book 38 volume is associated with Oncol. 10 (4) (2018) 528–533,
shorter length of stay
(2018) 708–715, [59] C. Grau, N. Defourny, J. Malicki, https://
and lower risks of re-admission
https://doi.org/10.1200/EDBK_ P. Dunscombe, J.M. Borras, M. doi.org/10.1016/j.jgo.2018.09.008.
and death: national cohort Coffey, et al.,
209089. [62] Y. Lievens, H. De Schutter, K.
analysis in England, Eur. J.
[36] K.A. Ung, B.A. Campbell, D. Radiotherapy equipment and Stellamans, M. Rosskamp, L. Van
Cancer 64 (2016) 32–43, departments in the European
Duplan, D. Ball, S. David, Eycken, Belgian College for
https://doi.org/10.1016/j.ejca.20 countries: final results from the
Impact of the lung oncology Physicians in Radiation Oncology,
16.05.021. ESTRO-HERO survey,
multidisciplinary team meetings Radiotherapy access in Belgium:
[44] M. Lüchtenborg, S.P. Riaz, V.H. Radiother. Oncol. 112 (2) (2014)
on the management of patients how far are we from evidence-
Coupland, E. Lim, E. Jakobsen, M. 155–164,
with Krasnik, et al., based utilisation? Eur. J. Cancer
https://doi.org/10.1016/j.radonc.2
014.08.029. 84 (2017)
High procedure volume is
strongly associated with [60] Y. Lievens, N. Defourny, M. 102–113,
improved survival after lung Coffey, J.M. Borras, P. https://doi.org/10.1016/j.ejca.2017.
cancer surgery, J. Clin. Oncol. 31 Dunscombe, B. Slotman, et al., 07.011.
(25) (2013) 3141–3146, [63] L.J. Taylor, J.D. Maloney, Moving
Radiotherapy staffing in the
https://doi.org/ European countries: final results beyond disease-focused decision
10.1200/JCO.2013.49.0219. making: understanding
from the ESTRO-
[45] H. Møller, V.H. Coupland, D. HERO survey, Radiother. Oncol. competing risks to personalize
Tataru, M.D. Peake, A. 112 (2) (2014) 178–186, lung cancer treatment for older
Mellemgaard, T. Round, et al., https://doi.org/ adults, J. Thorac. Dis. 9 (1) (2017)
Geographical variations in the 10.1016/j.radonc.2014.08.034. 8–12, https://doi.org/10.21037/
use of cancer treatments are
[61] L. Decoster, D. Schallier, jtd.2017.01.36.
associated with survival of lung
Treatment of older patients with [64] L.F. Forrest, J. Adams, H.
cancer patients, Thorax 73 (6)
advanced non-small cell lung Wareham, G. Rubin, M. White,
(2018) 530–537,
cancer: a challenge, J. Geriatr.
https://doi.org/ Socioeconomic inequalities in lung

23 8
T. Berghmans et al. Lung Cancer 150 (2020) 221–
cancer treatment: systematic https://www.cancerresearchuk.or 239 effectiveness
The
review and meta-analysis, PLoS g/sites/default/files/national_opti [83] M. Coory, P. Gkolia, I.A. Yang, of lung cancer MDT and the
Med. 10 (2) (2013) e1001376, mal_lung_pathway_aug_2017.pd R.V. Bowman, K.M. Fong, role of respiratory physicians,
https://doi.org/10.1371/journal.p f. Systematic review of Respirology 20 (6) (2015) 884–
med.1001376. [75] NHS Cancer Programme, multidisciplinary teams in the 888,
[65] A. Aggarwal, G. Lewison, S. Idir, Implementing a timed lung cancer management of lung cancer, https://doi.org/10.1111/resp.12
M. Peters, C. Aldige, W. diagnostic pathway, 2018. Lung Cancer 60 (1) (2008) 520.
Boerckel, The state of https://www.england.nhs.uk/wp- 14–21, [93] W.D. Travis, E. Brambilla, A.P.
lung cancer research: a content/uploads/2018/04/impleme https://doi.org/10.1016/j.lungc Burke, A. Marx, A.G. Nicholson,
global analysis, J. ntin g-timed-lung-cancer- an.2008.01.008. WHO Classification of Tumours
Thorac. Oncol. 11 (7) diagnostic-pathway.pdf. [84] C.J.L. Stone, H.M. Vaid, of the Lung, Pleura, Thymus and
(2016) 1040–1050, [76] Cancer Council Victoria, R. Selvam, A. Ashworth, Heart, fourth edition,
https://doi.org/10.1016/j.jt Optimal care pathway for A. Robinson, G.C. Digby, International Agency for
ho.2016.03.010. people with lung cancer, 2016. Multidisciplinary clinics in Research on Cancer, Lyon,
[66] A.L. Rich, L.J. Tata, C.M. Free, https://www.cancer.org.au/cont lung cancer care: a 2015.
R.A. Stanley, M.D. Peake, D.R. ent/ocp/health/optimal-care- systematic review, Clin. [94] W.D. Travis, E. Brambilla, M.
Baldwin, et al., How do patient pathway- for-people-with-lung- Lung Noguchi, A.G. Nicholson, K.
and hospital features influence cancer-june-2016.pdf. Geisinger, Y. Yatabe, et al.,
Cancer 19 (4) (2018) 323–330,
outcomes in small-cell lung [77] Cancer Care Ontario, Lung Cancer Diagnosis of lung cancer in
https://doi.org/10.1016/j.cllc.201
cancer Pathway Map, small biopsies and cytology:
8.02.001, e3.
in England? Br. J. Cancer 105 https://www.cancercareontar implications of the 2011
[85] H.A. Powell, D.R. Baldwin,
(6) (2011) 746–752,
io.ca/en/pathway-maps/lung- Multidisciplinary team International Association for the
https://doi.org/10.1038/ management in thoracic
bjc.2011.310. cancer. Study of Lung Cancer/American
[78] G. Fasola, S. Rizzato, V. Merlo, M. oncology: more than just a Thoracic Society/European
[67] B.R. Eaton, S.L. Pugh, J.D. concept? Eur. Respir. J. 43
Aita, T. Ceschia, F. Giacomuzzi, et Respiratory Society
Bradley, G. Masters, V.S. Kavadi, al., Adopting (6) (2014) 1776–1786,
S. Narayan, et al., Institutional classification, Arch. Pathol. Lab.
integrated care pathways in non- https://doi.org/10.1183/0903
enrollment and survival among 1936.00150813. Med. 137
small-cell lung cancer: from
NSCLC patients receiving theory to practice, J. Thorac. [86] E. Stone, N. Rankin, S. Kerr, (5) (2013) 668–684,
chemoradiation: NRG Oncology Oncol. 7 (8) (2012) 1283–1290, K. Fong, D.C. Currow, J. https://doi.org/10.5858/arpa.2012-
Radiation Therapy Oncology https://doi.org/10.1097/ Phillips, et al., Does 0263-RA.
Group (RTOG) 0617, J. Natl. JTO.0b013e318257fbfe. presentation at [95] Y. Yatabe, S. Dacic, A.C.
Cancer Inst. 108 (9) (2016), [79] G. Fasola, J. Menis, A. Follador, multidisciplinary team Borczuk, A. Warth, P.A.
https://doi.org/10.1093/jnci/djw03 E. De Carlo, F. Valent, G. Aresu, meetings improve lung Russell, S. Lantuejoul, et al.,
4. et al., Integrated care pathways in cancer survival? Best practices
[68] A.M. Forsea, Cancer registries in lung cancer: a quality Findings from a consecutive recommendations for
improvement project, Int. J. cohort study, Lung Cancer diagnostic
Europe – going forward is the 124 (2018) 199–204,
only option, Technol. immunohistochemistry in lung
https://doi.org/10.1016/j.lung
Ecancermedicalscience 10 Assess. Health Care 34 (1) (2018) cancer,
can.2018.07.032.
(2016) 641, 3–9, https://doi.org/10.1017/ J. Thorac. Oncol. 14 (3) (2019)
[87] N. Tamburini, P. Maniscalco, 377–407,
https://doi.org/10.3332/ S026646231700441X.
S. Mazzara, E. Maietti, A.
[80] A. Malalasekera, S. Nahm, P.L. https://doi.org/10.1016/j.
ecancer.2016.641. Santini, N. Calia, et al., jtho.2018.12.005.
Blinman, S.C. Kao, H.M. Dhillon,
[69] S. Siesling, W.J. Louwman, A. Multidisciplinary management [96] N.I. Lindeman, P.T. Cagle, D.L.
J.L. Vardy, How long is too long? A
Kwast, C. van den Hurk, M. improves survival at 1 year Aisner, M.E. Arcila, M.B.
scoping review of health system
O’Callaghan, S. Rosso, after surgical treatment for Beasley, E.H. Bernicker, et al.,
delays in lung cancer, Eur. Respir.
et al., Uses of cancer registries non-small-cell lung cancer: a Updated molecular testing
Rev. 27 (149) (2018) 180045,
for public health and clinical propensity score-matched guideline for the selection of
https://doi.org/10.1183/16000617.0
research in Europe: results of the study, Eur. lung cancer patients for
045- 2018.
European Network of Cancer J. Cardiothorac. Surg. 53 (6) treatment with targeted tyrosine
[81] C. Labb´e, M. Anderson, S. Simard, (2018) 1199–1204,
Registries survey among 161 L. Tremblay, F. Laberge, R. kinase inhibitors: guideline from
population-based cancer Vaillancourt, et al., https://doi.org/10.1093/ejcts/ the College of American
registries during 2010-2012, Eur. ezx464.
Wait times for diagnosis and Pathologists, the International
J. Cancer 51 (9) [88] T.V. Bilfinger, D. Albano,
treatment of lung cancer: a single- Association for the Study of
M. Perwaiz, R. Keresztes,
(2015) 1039–1049, centre experience, Curr. Oncol. Lung Cancer, and the
B. Nemesure, Survival
https://doi.org/10.1016/j.ejca.201 24 (6) (2017) 367–373, Association for Molecular
outcomes among lung
4.07.016. https://doi.org/10.3747/co.24.3655 Pathology, J. Mol. Diagn. 20 (2)
cancer patients treated
[70] A. Rich, P. Beckett, D. Baldwin, . (2018) 129–159,
Status of lung cancer data using a multidisciplinary
[82] European Partnership for Action https://doi.org/10.1016/j.jmoldx.20
collection in Europe, team
Against Cancer (EPAAC), approach, Clin. Lung Cancer 17.11.004.
JCO Clin. Cancer Inform. 2 (1)
(2018) 1–12, European Guide for Quality 19 (4) (2018) 346–351, [97] P.M. de Groot, J.H. Chung, J.B.
https://doi.org/10.1200/ National Cancer Control https://doi.org/10.1016/j. Ackman, M.F. Berry, B.W. Carter,
CCI.17.00052. Programmes, 2015, p. 30. cllc.2018.01.006. P.M. Colletti, et
[71] A. Rich, D. Baldwin, I. Alfageme, https://cancercontrol. [89] E. Jakobsen, T.R. Rasmussen, al., ACR Appropriateness
P. Beckett, T. Berghmans, S. eu/archived/uploads/images/Europ A. Green, Mortality and survival Criteria noninvasive clinical
of lung cancer in staging of primary lung cancer,
Brincat, et al., Achieving thoracic ean_Guide_for_Quality_National_C
Denmark: results from the J. Am. Coll. Radiol. 16 (5S)
oncology data collection in ancer (2019) S184–S195,
Europe: a precursor study in 35 _Control_Programmes_web.pdf. Danish Lung Cancer Group
2000-2012, Acta Oncol. 55 https://doi.org/10.1016/
countries, BMC Cancer 18 (1) j.jacr.2019.02.008.
(2018) 1144, (Suppl 2) (2016) 2–9,
[98] H. MacMahon, D.P. Naidich,
https://doi.org/10.1186/s12885- https://doi.org/10.3109/02841
J.M. Goo, K.S. Lee, A.N.C.
018-5009-y. 86X.2016.1150608.
Leung, J.R. Mayo, et al.,
[72] A.L. Rich, D.R. Baldwin, P. [90] German Cancer Society,
Guidelines for management of
Beckett, T. Berghmans, J. Boyd, Annual Report 2019 of the
incidental pulmonary nodules
C. Faivre-Finn, et al., ERS Certified Lung Cancer
detected on CT
statement on harmonised Centres, 2019.
images: from the Fleischner
standards for lung cancer http://www.ecc- Society 2017, Radiology 284
registration and lung cancer cert.org/certification- (1) (2017) 228–243,
services in Europe, Eur. Respir. system/document-collecti https://doi.org/10.1148/radiol.2
J. 52 (2018) 1800610, on. 017161659.
https://doi.org/ [91] SONCOS, Standardisation of [99] M.E. Callister, D.R. Baldwin, A.R.
Multidisciplinary Care in the Akram, S. Barnard, P. Cane, J.
10.1183/13993003.00610-2018.
Netherlands. SONCOS Draffan, et al.,
[73] National Institute for Health
Standardisation Report 5, British Thoracic Society
and Care Excellence. Lung guidelines for the
cancer overview, http 2017.
investigation and
s://pathways.nice.org.uk/path https://www.soncos.org/wp- management of pulmonary
ways/lung-cancer. content/up nodules, Thorax 70 (Suppl
[74] Lung Clinical Expert Group, loads/2017/10/46SONCOS- 2) (2015) ii1–ii54,
National Optimal Lung Cancer standardisation-report.pdf. https://doi.org/
Pathway, 2020 version 3.0, [92] C.N. Prabhakar, K.M. Fong, M.D. 10.1136/thoraxjnl-2015-
Peake, D.C. Lam, D.J. Barnes, 207168.

23 9
T. Berghmans et al. Lung Cancer 150 (2020) 221–
[100] F.C. Detterbeck, D.J. Boffa, for
18
FDG PET/CT restaging Berrisford, G. Rocco, Audit, 239
Sharouni,
A.W. Kim, L.T. Tanoue, The and treatment quality control, and performance M. Hatton, et al., Use of thoracic
eighth edition lung cancer response assessment in thoracic surgery – a European radiotherapy for extensive stage
stage classification, Chest 151 of malignant disease, perspective, Thorac. Surg. Clin. small-cell lung cancer: a phase 3
(1) (2017) 193–203, 17 (3) (2007) 387–393, randomised controlled trial,
J. Nucl. Med. 58 (12)
https://doi.org/10.1016/j. https://doi.org/10.1016/j.thorsurg Lancet 385 (9962) (2015) 36–42,
(2017) 2026–2037,
chest.2016.10.010. .2007.07.011. https://doi.org/10.1016/S0140-
https://doi.org/10.2967 [118] K.S. Albain, R.S. Swann, V.W.
[101] B.W. Carter, M.C. Godoy, 6736(14)61085-0.
/jnumed.117.197988. Rusch, A.T. Turrisi 3rd, F.A.
C.C. Wu, J.J. Erasmus, M.T. [126] D.R. Gomez, G.R. Blumenschein
Truong, Current [104] G. Ferna´ndez P´erez, R. Sa Shepherd, C. Smith, et
Jr, J.J. Lee, M. Hernandez, R. Ye,
controversies in lung cancer ´nchez-Escribano, A.M. García- al., Radiotherapy plus
D.R. Camidge, et al., Local
staging, J. Thorac. Imaging Vicente, A. Luna-Alcala´, chemotherapy with or without
consolidative therapy versus
31 (4) (2016) 201–214, J. Ceballlos-Viro, R.C. Delgado- surgical resection for stage III
Bolton, et al., SEOM-SERAM- maintenance therapy or
https://doi.org/10.1097/RTI.0 non-small-cell lung cancer: a
SEMNIM guidelines observation for
000000000000213. phase III randomised controlled
[102] R. Boellaard, R. Delgado-Bolton, on the use of functional and trial, Lancet 374 (9687) (2009)
W.J. Oyen, F. Giammarile, K. molecular imaging techniques
in advanced non-small cell 379–386,
Tatsch, https://doi.org/10.1016/S0140-
lung cancer, Clin. Transl.
W. Eschner, et al., FDG 6736(09)60737-6.
PET/CT: EANM procedure Oncol. 20 (7) (2018) 837–852,
https://doi.org/ [119] J.P. van Meerbeeck, G.W. Kramer,
guidelines for tumour
10.1007/s12094-017-1795-y. P.E. Van Schil, C. Legrand, E.F.
imaging: version 2.0, Eur. J.
[105] M. Majem, J. Hern´andez-Hern Smit,
Nucl. Med. Mol. Imaging 42
(2) (2015) 328–354, ´andez, F. Hernando-Trancho, N. F. Schramel, et al., Randomized
Rodríguez de Dios, controlled trial of resection versus
https://doi.
org/10.1007/s00259-014- A. Sotoca, J.C. Trujillo-Reyes, et radiotherapy after induction
2961-x. al., Multidisciplinary consensus chemotherapy in stage IIIA-N2
[103] H. Jadvar, P.M. Colletti, R. statement on the clinical non-small-cell lung cancer, J.
Delgado-Bolton, G. Esposito, management of patients with Natl.
B.J. Krause, A.H. Iagaru, et
stage III non-small cell lung Cancer Inst. 99 (6) (2007) 442–
al., Appropriate use criteria
cancer, Clin. 450,
10.1093/annonc/mdt178. https://doi.org/10.1093/jnci/djk0
Transl. Oncol. 22 (1) (2019) 21– [111] N.M. deSouza, Y. Liu, A. Chiti, D. 93.
Oprea-Lager, G. Gebhart, B.E. [120] L. Crino`, W. Weder, J. van
36, Meerbeeck, E. Felip, ESMO
Van Beers, et al., Strategies and
https://doi.org/10.1007/s12094- Guidelines Working Group,
technical challenges for imaging
019-02134- oligometastatic disease: Early stage and locally advanced
7. (non-metastatic) non-small-cell
recommendations from the
[106] R.C. Delgado Bolton, A.K. lung cancer:
European Organisation for
Calapaquí-Tera´n, F. Giammarile, ESMO Clinical Practice
D. Rubello, Role of Research and Treatment of Guidelines for diagnosis,
18 Cancer imaging group, Eur.
F-FDG PET/CT in treatment and follow-up, Ann.
J. Cancer 91 (2018) 153–
establishing new clinical and Oncol. 21 (Suppl 5) (2010)
163, https://doi.org/
therapeutic modalities in lung v103–115,
10.1016/j.ejca.2017.12.012.
cancer. A short review, Rev. https://doi.org/10.1093/annonc/
Esp. Med. Nucl. Imagen Mol. 38 [112] F.F. Chen, D. Zhang, Y.L. Wang,
B. Xiong, Video-assisted mdq207.
(4) (2019) 229–233,
thoracoscopic surgery lobectomy [121] C. Faivre-Finn, S. Falk, F.
https://doi.org/10.1016/j.remn.2 Blackhall, The CONVERT trial:
019.02.003. versus open lobectomy in patients
interpretation, journey and
[107] W.E.E. Eberhardt, D. De with clinical stage I non-small cell
lessons learnt, Clin. Oncol. (R
Ruysscher, W. Weder, C. Le lung cancer: a meta-analysis,
Coll Radiol) 29 (12) (2017) 811–
Pechoux, P. De Leyn, Eur. J. Surg. Oncol. 39 (9)
(2013) 957–963, https:// 813, https://
H. Hoffmann, et al., 2nd ESMO doi.org/10.1016/j.clon.2017.09.0
Consensus Conference in Lung doi.org/10.1016/j.ejso.2013.06.0
16. 02.
Cancer: locally
[113] S. Wei, M. Chen, N. Chen, L. Liu, [122] D. De Ruysscher, B. Lueza, C. Le
advanced stage III non- P´echoux, D.H. Johnson, M.
small-cell lung cancer, Feasibility and safety of robot-
O’Brien, N. Murray, et al., Impact
Ann. Oncol. 26 (8) (2015) assisted thoracic surgery for lung
of thoracic radiotherapy timing in
1573–1588, lobectomy in patients with non- limited-stage small-cell lung
https://doi.org/10.1093/an small cell lung cancer: a cancer: usefulness of the
nonc/mdv187. systematic review and meta- individual patient data meta-
[108] U. Nestle, D. De Ruysscher, U. analysis, World J. Surg. Oncol. 15 analysis, Ann. Oncol. 27 (10)
Ricardi, X. Geets, J. Belderbos, C. (1) (2017) 98, (2016) 1818–1828,
Po¨ttgen, et al., https://doi.org/10.1186/s12957- https://doi.org/10.1093/annonc/
ESTRO ACROP guidelines for 017-1168-6. mdw263.
target volume definition in the [114] P.H. Schipper, B.S. Diggs, R.M. [123] J.D. Bradley, R. Paulus, R.
treatment of locally advanced Ungerleider, K.F. Welke, The
Komaki, G. Masters, G.
non-small cell lung cancer, influence of surgeon
Radiother. Oncol. 127 (1) Blumenschein, S. Schild, et al.,
specialty on outcomes in general
(2018) 1–5, thoracic surgery: a national Standard-dose versus high-dose
https://doi.org/10.1016/j.radonc. sample 1996 to 2005, Ann. conformal radiotherapy with
2018.02.023. Thorac. Surg. 88 (5) (2009) concurrent and consolidation
[109] D. De Ruysscher, C. Faivre-Finn, 1566–1572, carboplatin plus paclitaxel with or
D. Moeller, U. Nestle, C.W. https://doi.org/10.1016/j. without cetuximab for patients
Hurkmans, C. Le P´echoux, et athoracsur.2009.08.055. with stage IIIA or IIIB non-small-
al., European Organization for [115] F. Farjah, D.R. Flum, T.K. cell lung cancer (RTOG 0617): a
Research and Treatment of Varghese Jr, R.G. Symons, D.E. randomised,
Cancer (EORTC) Wood, Surgeon specialty and two-by-two factorial phase
long-term survival after 3 study, Lancet Oncol. 16
recommendations for planning
pulmonary resection for lung (2) (2015) 187–199,
and delivery of high-dose, high
cancer, Ann. https://doi.org/10.1016/S14
precision 70-2045(14)71207-0.
radiotherapy for lung cancer, Thorac. Surg. 87 (4) (2009) 995– [124] P.E. Postmus, K.M. Kerr, M.
Radiother. Oncol. 124 (1) 1004, https://doi.org/10.1016/j.
(2017) 1–10, https://doi. athoracsur.2008.12.030. Oudkerk, S. Senan, D.A. Waller,
org/10.1016/j.radonc.2017.06.0 [116] K.K. Lau, S. Rathinam, D.A. J. Vansteenkiste, et al., Early and
03. Waller, M.D. Peake, The effects of locally advanced non-small-cell
[110] M. Früh, D. De Ruysscher, S. increased provision of thoracic lung cancer (NSCLC): ESMO
Popat, L. Crino`, S. Peters, E. surgical specialists on the Clinical Practice Guidelines for
Felip, et al., Small-cell diagnosis, treatment and follow-
variation in lung cancer resection
lung cancer (SCLC): ESMO up, Ann. Oncol.
rate in
clinical practice guidelines for 28 (suppl_4) (2017) iv1–iv21,
England, J. Thorac. Oncol. 8 (1)
diagnosis, treatment and
(2013) 68–72, https://doi.org/10.1093/annonc/m
follow-up, Ann. Oncol. 24
(Suppl. 6) (2013) vi99–vi105, https://doi.org/10.1097/ dx222.
JTO.0b013e3182762315. [125] B.J. Slotman, H. van Tinteren,
https://doi.org/ [117] A. Brunelli, G. Varela, R. J.O. Praag, J.L. Knegjens, S.Y. El

23 1
T. Berghmans et al. Lung Cancer 150 (2020) 221–
The role of advanced nursing in 4039–4045, 239
Reynolds, C.J. Langer,
patients with oligometastatic non- lung cancer: a framework based https://doi.org/10.21037/ Caring for the older
small-cell lung cancer without development, jtd.2017.08.142. population with advanced
progression after Eur. J. Oncol. Nurs. 19 (6) (2015) lung cancer, Am. Soc. Clin.
[143] M. Radovic, R. Kanesvaran, A.
740–746, Oncol. Educ. Book 37 (2017)
first-line systemic therapy: a Rittmeyer, M. Früh, F. Minervini,
M. Glatzer, et al., 587–596,
multicentre, randomised, https://doi.org/10.1016/j.
ejon.2015.05.009. Multidisciplinary treatment of https://doi.org/10.1200/EDBK
controlled, phase 2 study,
[135] T.J.P. Batchelor, N.J. Rasburn, E. _179850.
Lancet Oncol. 17 (12) (2016) lung cancer in older patients: a
Abdelnour-Berchtold, A. Brunelli, [146] A. Petit-Mon´eger, M. Rainfray,
1672–1682, review, J. Geriatr. Oncol. 10
R.J. Cerfolio, P. Soubeyran, C.A. Bellera, S.
https://doi.org/10.1016/S1470- (3) (2018) 405–410,
M. Gonzalez, et al., Guidelines Mathoulin-P´elissier, Detection
2045 https://doi.org/10.1016/j.jgo.20
for enhanced recovery after lung of frailty in elderly cancer
(16)30532-0. 18.09.005.
surgery: recommendations of the [144] R. Corre, L. Greillier, H. Le patients: improvement of the G8
[127] P. Iyengar, Z. Wardak, D.E. Enhanced Recovery After
Ca¨er, C. Audigier-Valette, N. screening
Gerber, V. Tumati, C. Ahn, Surgery (ERAS) Society and the test, J. Geriatr. Oncol.
R.S. Hughes, et al., Baize, H. B´erard, et al., Use of 7 (2) (2016) 99–107,
European Society of Thoracic
Consolidative radiotherapy a comprehensive geriatric https://doi.org/10.1016/
Surgeons (ESTS), Eur. J.
for limited metastatic non- assessment for the j. jgo.2016.01.004.
Cardiothorac. Surg. 55
small-cell lung cancer: a management of elderly [147] H. Wildiers, P. Heeren, M. Puts, E.
(1) (2019) 91–115, patients with advanced non-
phase 2 randomized clinical Topinkova, M.L. Janssen-Heijnen,
https://doi.org/10.1093/ejcts/ezy3 small-cell lung cancer: the M. Extermann, et al.,
trial, JAMA Oncol. 4 (1)
01. phase III randomized International Society of Geriatric
(2018) e173501, https://
[136] T.P. Chamogeorgakis, C.P. Oncology consensus on geriatric
doi.org/10.1001/jamaoncol.2 Connery, F. Bhora, A. Nabong, I.K. ESOGIA-GFPC-GECP 08-02
017.3501. Toumpoulis, study, J. Clin. Oncol. 34 (13) assessment in older patients with
[128] R. Arriagada, A. Dunant, J.P. (2016) 1476–1483, cancer, J. Clin. Oncol. 32 (24)
Thoracoscore predicts midterm
Pignon, B. Bergman, M. mortality in patients https://doi.org/10.1200/JCO.2015 (2014) 2595–2603,
Chabowski, D. Grunenwald, et undergoing thoracic surgery, J. .63.5839. https://doi.org/10.1200/JCO.2013
al., Long-term results of the Thorac. Cardiovasc. Surg. 134 [145] C.J. Presley, C.H. .54.8347.
international adjuvant lung (4) (2007) 883–887, man.2016.12.338.
cancer trial evaluating adjuvant https://doi.org/10.1016/j. [155] O.P. Geerse, J.E. Hoekstra-
[148] S. Borson, J.M. Scanlan, P. Chen,
cisplatin-based chemotherapy jtcvs.2007.06.020. Weebers, M.H. Stokroos, J.G.
M. Ganguli, The Mini-Cog as a
in resected lung cancer, J. Clin. [137] E. Duka, A.M. Ierardi, C. screen for Burgerhof, H.J. Groen, H.
Oncol. 28 Floridi, A. Terrana, F. Fontana, dementia: validation in a A. Kerstjens, et al., Structural
G. Carrafiello, The role of distress screening and supportive
(1) (2010) 35–42, population-based sample, J. Am.
interventional oncology in the care for patients
https://doi.org/10.1200/JCO.200 Geriatr. Soc. 51 (10) (2003)
management of lung cancer, with lung cancer on systemic
9.23.2272. 1451–1454,
Cardiovasc. Intervent. Radiol. therapy: a randomised controlled
[129] E. Lim, G. Harris, A. Patel, I. https://doi.org/10.1046/j.1532-
40 (2) (2017) 153–165, trial, Eur. J. Cancer 72 (2017) 37–
Adachi, L. Edmonds, F. Song, 5415.2003.51465.x.
https://doi.org/10.1007/s00270- 45,
Preoperative versus [149] European Society of
016-1495-y. https://doi.org/10.1016/j.ejca.2016
postoperative chemotherapy in Oncology Pharmacy, Quality
[138] D. Yaffe, M. Koslow, H. Haskiya, .11.006.
patients with resectable non- Standard for the Oncology
D. Shitrit, A novel technique for [156] J.R. Rueda, I. Sol`a, A. Pascual,
small cell lung cancer: Pharmacy Service (QuapoS
CT-guided M. Subirana Casacuberta, Non-
systematic review and indirect 6), 2018.
transthoracic biopsy of lung invasive interventions for
comparison meta-analysis of https://esop.li/quapos.
lesions: improved biopsy improving well-being and quality
randomized [150] J. Zabora, K. BrintzenhofeSzoc, B.
accuracy and safety, Eur. of life in patients with lung
trials, J. Thorac. Oncol. 4 (11) Curbow, C. Hooker, S. Piantadosi,
Radiol. 25 (11) (2015) 3354– The cancer, Cochrane Database
(2009) 1380–1388,
3360, prevalence of psychological Syst. Rev. 9 (2011) CD004282,
https://doi.org/10.1097/
JTO.0b013e3181b9ecca. https://doi.org/10.1007/s00330- distress by cancer site, https://doi.org/
[130] A. Aup´erin, C. Le P´echoux, E. 015-3750-z. Psychooncology 10 (1) (2001) 10.1002/14651858.CD004282.p
Rolland, W.J. Curran, K. Furuse, [139] P.L. Pereira, S. Masala, 19–28, ub3.
P. Fournel, et al., Standards of practice: guidelines https://www.ncbi.nlm.nih.gov/pub [157] C.G. Brown Johnson, J.L. Brodsky,
Meta-analysis of concomitant for thermal ablation of primary J.K. Cataldo, Lung cancer stigma,
med/11180574.
versus sequential anxiety,
and secondary lung tumors, [151] S.L. Sanders, E.O. Bantum, J.E.
radiochemotherapy in locally depression, and quality of life, J.
Cardiovasc. Intervent. Radiol. Owen, A.A. Thornton, A.L. Psychosoc. Oncol. 32 (1) (2014)
advanced non-small-cell lung
35 (2) (2012) Stanton, Supportive care needs in 59–73, https://
cancer, J. Clin. Oncol. 28 (13)
247–254, patients with lung cancer, doi.org/10.1080/07347332.2013.8
(2010) 2181–2190, Psychooncology 19 (5) (2010)
https://doi.org/10.1007/s00270- 55963.
https://doi.org/10.1200/JCO.20 480–489,
09.26.2543. 012-0340-1. [158] National Comprehensive Cancer
https://doi.org/10.1002/pon.1577. Network, Distress management.
[131] L. Horn, A.S. Mansfield, A. [140] D.E. Dupuy, H.C. Fernando,
[152] T. Steinberg, M. Roseman, G. Clinical practice guidelines, J.
Szczęsna, L. Havel, M. S. Hillman, T. Ng, A.D. Tan,
Kasymjanova, S. Dobson, L. Compr. Canc. Netw. 1 (3) (2003)
Krzakowski, M.J. Hochmair, et A. Sharma, et al., Lajeunesse, 344–374, http://www.jnccn.org/c
al., First-line atezolizumab plus Radiofrequency ablation of E. Dajczman, et al., ontent/1/3/344.long.
chemotherapy in extensive- stage IA non-small cell lung Prevalence of emotional [159] C.L. Granger, Physiotherapy
stage small-cell lung cancer in medically distress in newly diagnosed management of lung cancer, J.
cancer, N. Engl. J. Med. 379 inoperable patients: results lung cancer patients, Support.
Care Cancer 17 (12) (2009) Physiother. 60 (4) (2016) 181–
(23) (2018) 2220–2229, from the American College
1493–1497, https://doi. 188,
https://doi.org/10.1056/ of Surgeons Oncology
NEJMoa1809064. https://doi.org/10.1016/j.jphys.2
Group Z4033 (Alliance) trial, org/10.1007/s00520-009-
[132] University of Nottingham, Cancer 121 (19) (2015) 3491– 0614-6. 014.08.018.
Care provided by 3498, https://doi. [153] C. Lo, C. Zimmermann, A. [160] H. Rivas-Perez, P. Nana-
specialist cancer nurses org/10.1002/cncr.29507. Rydall, A. Walsh, J.M. Sinkam, Integrating pulmonary
helps improve life [141] B.Y. Huang, X.M. Li, X.Y. Song, Jones, M.J. Moore, et al., rehabilitation into the
expectancy of patients J.J. Zhou, Z. Shao, Z.Q. Yu, et Longitudinal study of multidisciplinary management
with lung cancer, says al., Long-term results of CT- depressive symptoms in of lung cancer: a review,
new study, Press release guided percutaneous patients with metastatic Respir. Med. 109 (4)
4 July, 2018. radiofrequency ablation of gastrointestinal and lung (2015) 437–442,
https://bit.ly/2I56zQa. inoperable patients with stage Ia cancer, J. Clin. Oncol. 28 https://doi.org/10.1016/j.rmed.201
non-small cell lung cancer: a (18) (2010) 3084–3089,
[133] A. Serena, A.A. Dwyer, S. 5.01.001.
retrospective cohort study, Int. J. https://doi.org/10.1200/JCO. [161] V. Cavalheri, C. Burtin, V.R.
Peters, M. Eicher, Acceptance
2009.26.9712.
of the advanced practice nurse Surg. Formico, M.L. Nonoyama, S.
[154] A. Vodermaier, S. Lucas, W.
in lung cancer role by 53 (2018) 143–150, Jenkins, M.A. Spruit, et al.,
Linden, R. Olson, Anxiety after
healthcare professionals and https://doi.org/10.1016/j.ijsu.2018 Exercise training undertaken by
diagnosis predicts lung cancer-
patients: a qualitative .03.034. people within 12 months of lung
specific and overall survival in
exploration, J. Nurs. Scholarsh. [142] C.K. Narsule, P. Sridhar, D. Nair, resection for non-small cell lung
50 (5) (2018) 540–548, patients with stage III non-small
A. Gupta, R.G. Oommen, M.I. cancer, Cochrane Database Syst.
https://doi.org/10.1111/ Ebright, et al., cell lung cancer: a population-
Rev. 6 (2019) CD009955,
jnu.12411. Percutaneous thermal ablation based cohort study, J. Pain
https://doi.org/10.1002/14651858.
[134] A. Serena, P. Castellani, N. for stage IA non-small cell lung Symptom Manage. 53 (6)
CD009955.pub3.
Fucina, A.C. Griesser, J. cancer: long-term follow-up, J. (2017) 1057–1065, [162] C.J. Peddle-McIntyre, F. Singh, R.
Jeanmonod, S. Peters, et al., Thorac. Dis. 9 (10) (2017) https://doi.org/10.1016/j.jpainsym Thomas, R.U. Newton, D.A.

23 1
T. Berghmans et al. Lung Cancer 150 (2020) 221–
Galva˜o, population-based study using 239
https://www.ncbi.nlm.nih.gov/pmc/articl
V. Cavalheri, Exercise training for [170] P. Bhattacharya, S.K. Dessain, routinely available data, Int. J. es/PMC5094603.
advanced lung cancer, Cochrane T.L. Evans, Palliative care in Qual. [190] S. Ekman, F. Griesinger, P.
Database Syst. Rev. 2 (2019) Health Care 30 (4) (2018) 306– Baas, D. Chao, C. Chouaid, J.C.
lung cancer: when to start,
CD012685, O’Donnell, et al., I-O Optimise: a
Curr. Oncol. Rep. 20 (11) 312,
https://doi.org/10.1002/1465185 novel multinational real-world
(2018) 90, https://doi.org/10.1093/intqhc/m research platform in thoracic
8.CD012685.pub2. https://doi.org/10.1007/s11912- zy027. malignancies, Future
[163] F. Boujibar, T. Bonnevie, D. 018- 0731-9. [181] Belgian Health Care Knowledge Oncol. 15 (14) (2019)
Debeaumont, M. Bubenheim, A. [171] M. Villalobos, A. Siegle, L. centre (KCE), Quality Indicators 1551–1563,
Cuvellier, C. Peillon, et al., Hagelskamp, C. Jung, M. for the Management of Lung https://doi.org/
Impact of prehabilitation on Thomas, Communication along Cancer. KCE Reports 266, 10.2217/fon-2019-0025.
morbidity and mortality after milestones in lung cancer 2016. https://kce.fgov.be/en/qua
pulmonary lobectomy by patients with advanced disease, lity-indicators-for-the-
minimally invasive surgery: a Oncol. Res. Treat. management-of-lung-cancer.
cohort study, J. Thorac. Dis. 10 [182] M. Ten Berge, N. Beck, D.J.
42 (1–2) (2019) 41–46,
(4) Heineman, R. Damhuis, W.H.
https://doi.org/10.1159/00049640
(2018) 2240–2248, Steup, P.J. van Huijstee, et al.,
7.
https://doi.org/10.21037/jtd.2018 [172] B.R. Ferrell, J.S. Temel, S. Dutch Lung Surgery Audit: a
.03.161. Temin, E.R. Alesi, T.A. Balboni, national audit comprising lung
[164] L. Zeng, X. Yu, T. Yu, J. Xiao, E.M. Basch, et al., Integration of and thoracic
Y. Huang, Interventions for palliative care into standard surgery patients, Ann. Thorac.
smoking cessation in people Surg. 106 (2) (2018) 390–397,
oncology care: American
diagnosed with lung cancer, https://doi.org/
Society of Clinical Oncology
Cochrane Database Syst. Rev. 10.1016/j.athoracsur.2018.03.04
clinical practice guideline 9.
6 (2019) CD011751, update, J. Clin. Oncol. 35 (1) [183] N. Beck, F. Hoeijmakers, E.M.
https://doi.org/10.1002/146518 (2017) Wiegman, H.J.M. Smit, F.M.
58.CD011751.pub3.
96–112, Schramel, W.H. Steup, et al.,
[165] M.W. Haun, S. Estel, G. Rücker,
https://doi.org/10.1200/JCO.2016 Lessons learned from the Dutch
H.C. Friederich, M. Villalobos, M.
.70.1474. Institute for Clinical Auditing: the
Thomas, et al., Early palliative [173] T.E. Quill, A.P. Abernethy, Dutch model for quality
care for adults with advanced Generalist plus specialist
assurance in lung cancer
cancer, Cochrane Database Syst. palliative care – creating a
treatment, J. Thorac. Dis. 10
Rev. 6 (2017) CD011129, more sustainable model, N.
Engl. J. Med. 368 (13) (2013) (Suppl
https://doi.org/10.1002/14651858.
1173–1175, https:// 29) (2018) S3472–S3485,
CD011129.pub2.
doi.org/10.1056/NEJMp12156 https://doi.org/10.21037/jtd.2018.
[166] D. Kavalieratos, J. Corbelli, D. 20.
Zhang, J.N. Dionne-Odom, N.C. 04.56.
[174] L. Evans, B. Donovan, Y. [184] E. Stone, N. Rankin, J. Phillips,
Ernecoff,
Liu, T. Shaw, P. Harnett, A K. Fong, D.C. Currow, A. Miller,
J. Hanmer, et al., Association
between palliative care and tool to improve the et al., Consensus minimum data
patient and caregiver performance of set for lung cancer
outcomes: a systematic multidisciplinary teams in multidisciplinary teams: results
review and meta- cancer care, BMJ Open of a Delphi
analysis, JAMA 316 (20) Qual. 8 (2) (2019) e000435, process, Respirology 23 (10)
(2016) 2104–2114, https://doi.org/10.1136/bmjo (2018) 927–934,
https://doi.org/10.1001/ja q-2018-000435. https://doi.org/10.1111/
ma.2016.16840. [175] E. Stone, N.M. Rankin, S.K. resp.13307.
[167] M.S. Aapro, Supportive care Vinod, M. Nagarajah, C. [185] K.S. Mak, A.C. van Bommel, C.
and palliative care: a time for Donnelly, D.C. Currow, et al., Stowell, J.L. Abrahm, M. Baker,
unity in diversity, Ann. Oncol. Clinical impact of data feedback C.S. Baldotto, et al., Defining a
23 (8) (2012) 1932–1934, at lung cancer multidisciplinary standard set of patient-centred
https://doi.org/10.1093/annonc/ team meetings: a outcomes for lung cancer, Eur.
mds239. mixed methods study, Asia. J. Respir. J. 48 (3) (2016) 852–860,
[168] K. Jordan, M. Aapro, S. Kaasa, Clin. Oncol. 16 (2020) 45–45, https://doi.org/10.1183/13993003
C.I. Ripamonti, F. Scott´e, F. https://doi.org .02049-
Strasser, et al., /10.1111/ajco.13278. 2015.
European Society for Medical [176] F. Denis, E. Basch, A.L. [186] M. Koller, M.J. Hjermstad, K.A.
Oncology (ESMO) position Septans, J. Bennouna, T. Tomaszewski, I.M. Tomaszewska,
paper on supportive and Urban, A.C. Dueck, et al., Two- K. Hornslien,
palliative care, Ann. Oncol. 29 A. Harle, et al., An international
year survival comparing web-
(1) (2018) 36–43, study to revise the EORTC
based symptom monitoring vs
https://doi.org/10.1093/ questionnaire for assessing quality
routine surveillance
annonc/mdx757. of life in lung cancer patients, Ann.
following treatment for lung
[169] J.S. Temel, J.A. Greer, A. cancer, JAMA 321 (3) (2019) Oncol. 28 (11) (2017)
Muzikansky, E.R. Gallagher, S. 306–307, https://doi. 2874–2881,
Admane, V.A. Jackson, et al., org/10.1001/jama.2018.18085. https://doi.org/10.1093/annonc/m
Early palliative care for patients [177] A. Wind, A. Rajan, W.H. van dx453.
with metastatic non-small-cell Harten, Quality assessments for [187] F. Gamarra, J.L. No¨el, A.
lung cancer, cancer centers in the European Brunelli, A.C. Dingemans, E.
N. Engl. J. Med. 363 (8) (2010) Union, BMC Health Serv. Res. Felip, M. Gaga, et al.,
733–742, Thoracic oncology HERMES:
16 (2016) 474,
https://doi.org/10.1056/ https://doi.org/10.1186/ s12913- European curriculum
NEJMoa1000678.
016-1738-2. recommendations for training
[178] NICE, Lung cancer in adults. in thoracic oncology, Breathe
QS17, 2019. 12 (3) (2016) 249–255,
https://www.nice.org.uk/guidan https://doi.org/10.1183/
ce/ qs17. 20734735.009116.
[179] Royal College of Physicians, [188] K. Benstead, N.S. Turhal, N.
National Lung Cancer Audit O’Higgins, L. Wyld, M.
annual report 2018 (for the Czarnecka-Operacz,
audit period 2017), 2019. H. Gollnick, et al.,
https://www.rcplondon.ac.uk/pr Multidisciplinary training of
ojects/outpu ts/nlca-annual- cancer specialists in Europe, Eur.
report-2018. J. Cancer 83 (2017) 1–8,
[180] F. Vrijens, C. De Gendt, L. https://doi.org/10.1016/j.ejca.201
Verleye, J. Robays, V. 7.05.043.
Schillemans, C. Camberlin, et [189] E. Jakobsen, T.R. Rasmussen,
al., Quality of care and variability The Danish Lung Cancer
in lung cancer management Registry, Clin. Epidemiol.
across Belgian hospitals: a 8 (2016) 537–541.

23 1

You might also like