Open access Original research Oncological care organisation during COVID-19 outbreak Concetta Elisa Onesti ‍ ,1,2 Hope S Rugo,3 Daniele Generali,4,5 Marc Peeters ‍ ,6 Khalil Zaman,7 Hans Wildiers,8 Nadia Harbeck,9 Miguel Martin,10 Massimo Cristofanilli,11 Javier Cortes,12,13 Vivianne Tjan-­Heijnen,14 Sara A Hurvitz,15 Guy Berchem,16 Marco Tagliamento ‍ ,17 Mario Campone,18 Rupert Bartsch,19 Sabino De Placido,20 Fabio Puglisi ‍ ,21 Sylvie Rottey,22 Volkmar Müller,23 Thomas Ruhstaller,24 Jean-­Pascal Machiels,25 PierFranco Conte,26,27 Ahmad Awada,28,29 Guy Jerusalem1,30 ►► Additional material is ABSTRACT published online only. To view, Key questions Background COVID-19 appeared in late 2019, causing a please visit the journal online pandemic spread. This led to a reorganisation of oncology (http://​dx.​doi.​org/​10.​1136/​ What is already known about this subject? care in order to reduce the risk of spreading infection esmoopen-​2020-​000853). ►► The COVID-19 pandemic led to a reorganisation of between patients and healthcare staff. Here we analysed oncological care, based on expert advice, in order to To cite: Onesti CE, Rugo HS, measures taken in major oncological units in Europe and reduce the spread of infection between patients and Generali D, et al. Oncological the USA. healthcare staff. care organisation during Methods A 46-­item survey was sent by email to COVID-19 outbreak. ESMO Open representatives of 30 oncological centres in 12 of the most What does this study add? 2020;5:e000853. doi:10.1136/ affected countries. The survey inquired about preventive ►► The practical aspects of managing patients with esmoopen-2020-000853 measures established to reduce virus spread, patient cancer in multiple cancer centres during the education and processes employed for risk reduction in COVID-19 health crisis have been analysed in this Received 2 June 2020 each oncological unit. report. Many pragmatic measures have been quickly Revised 8 July 2020 Results Investigators from 21 centres in 10 countries implemented, although the relative efficacy of each Accepted 13 July 2020 answered the survey between 10 April and 6 May 2020. intervention should be further analysed in large ob- A triage for patients with cancer before hospital or servational studies. Published online clinic visits was conducted by 90.5% of centres before 26 August 2020 consultations, 95.2% before day care admissions and in How might this impact on clinical practice? 100% of the cases before overnight hospitalisation by ►► This analysis could be extremely interesting from means of phone calls, interactive online platforms, swab an organisational point of view for possible future test and/or chest CT scan. Permission for caregivers to epidemics, for countries actually at the peak of the attend clinic visits was limited in many centres, with some pandemic and in case a second COVID-19 peak oc- exceptions (ie, for non-­autonomous patients, in the case curs in the next months. of a new diagnosis, when bad news was expected and for terminally ill patients). With a variable delay period, the use of personal protective equipment was unanimously China.1 The causative agent was identified mandatory, and in many centres, only targeted clinical and as a new coronavirus, called SARS-­ CoV-2, instrumental examinations were performed. Telemedicine phylogenetically similar to SARS-­ CoV-1, was implemented in 76.2% of the centres. Separated responsible for the SARS outbreak that pathways for COVID-19-­positive and COVID-19-­negative occurred in 2002.2 SARS-­CoV-2 derives from patients were organised, with separate inpatient units and day care areas. Self-­isolation was required for COVID-19-­ natural selection likely in bats or pangolins positive or symptomatic staff, while return to work policies with zoonotic transfer, leading to high affinity required a negative swab test in 76.2% of the centres. binding to the human ACE2 receptor.3 © Author (s) (or their Conclusion Many pragmatic measures have been COVID-19 infection has rapidly spread and employer(s)) 2020. Re-­use quickly implemented to deal with the health emergency was declared a pandemic by the WHO on permitted under CC BY-­NC. No linked to COVID-19, although the relative efficacy of 11 March 2020. More than five million cases commercial re-­use. Published each intervention should be further analysed in large and more than 300 000 deaths have been by BMJ on behalf of the European Society for Medical observational studies. reported in May worldwide.4 Several coun- Oncology. tries have adopted measures to limit virus For numbered affiliations see INTRODUCTION spread, including lockdown, social distancing end of article. A novel coronavirus disease, named COVID- and reinforcement of hygiene requirements. Correspondence to 19, responsible for SARS, appeared in late Hospital activities have also been reorgan- Dr Concetta Elisa Onesti; 2019, originating most likely from a seafood ised in order to reduce the risk of contagion ​elisaonesti@​gmail.​com market in Wuhan, in the Hubei province of among patients and caregivers. Onesti CE, et al. ESMO Open 2020;5:e000853. doi:10.1136/esmoopen-2020-000853 1 Open access Patients with cancer belong to a high-­risk category for practices, modification of diagnostic technologies and complications from infection due to organ damage from from national regulations on the availability and applica- both tumour growth and treatment toxicity, immunosup- bility of tests and isolation procedures. pression resulting from tumour and anticancer therapies, The data obtained are presented as a percentage of and the generally advanced age group and presence of responses out of the total number of participating centres, frequent comorbidities. Moreover, patients with cancer and bar chart was used to summarise data on triage, require frequent access to the hospital for assessment of screening and general measures taken for risk reduction disease status and toxicity, and in order to receive appro- and specific measures in inpatient units. priate care, with increased risk of exposure to germs. The burden on the health system for each country at An analysis of 1524 patients admitted to a radiation the moment of the survey completion was reported as and medical oncology unit in Wuhan from December the number of affected cases per 100 000 inhabitants, 2019 to February 2020 found a twofold increase of the with data extracted from the Johns Hopkins University risk of COVID-19 infection rate in patients with cancer COVID-19 Data Repository.4 compared with the general population (0.79% vs 0.37%) over the same period of time.5 Data derived from a nation- wide analysis in China reported that COVID-19-­positive RESULTS patients with cancer (N=18) had a higher risk of severe Between 10 April and 6 May 2020, a total of 21 institu- events compared with patients without cancer (39% vs tions from 10 different countries answered the survey by 8%, p=0.0003), especially patients in active treatment email: from Belgium (5), Italy (4), Spain (2), Germany compared with cancer survivors.6 In an Italian cohort (2), Switzerland (2), USA (2), Austria (1), the Nether- published last March, 72 deaths out of 355 (20.3%) lands (1), France (1) and Luxembourg (1). Overall, 15 occurred in patients with cancer, while only 0.8% of centres were university general hospitals, 5 were compre- the deaths occurred in patients without comorbidities, hensive cancer centres and 1 was a private clinic. All the including cancer.7 centres included experienced high-­capacity oncological Facing this exceptional and rapidly developing situa- units. Among these, 21 centres had consultations and day tion, no standard operating procedures for care organ- care facilities, and 20 had an overnight facility. isations existed in oncologiocal institutions, although The burden of COVID-19 cases on the health system is general recommendations for healthcare in hospital calculated as the number of total infections per 100 000 units, for COVID-19 and suspected case management inhabitants in each country (figure 1). However, consid- were rapidly drafted.8 Several recent expert statements ering the different applicability of the test in the acute have been published addressing how to manage care in phase of the outbreak in different countries, the number specialist oncology departments, but few reports guide of cases does not fully reflect the real load of infection. At effective organisation for daily clinical practice.9–20 We the moment of survey completion, a lower burden, with aimed to assess how oncology centres and departments less than 200 cases per 100 000 inhabitants, was observed reacted to the health crisis related to the COVID-19 for France, Germany, Austria, the Netherlands and one pandemic, in order to improve oncological care and to centre from USA. For Italy, Belgium, Switzerland, Spain implement preventive measures. and the other centre from USA, 200–400 patients were affected by COVID-19 per 100 000 inhabitants. The most affected country was Luxembourg, with more than 500 MATERIALS AND METHODS cases per 100 000 inhabitants. A survey (online supplementary material) was sent by email to 30 representatives of oncological departments in Triage, screening procedures and patients’ education 12 of the most affected countries by COVID-19 in Europe Patients were subjected to a triage for signs of infection and the USA in order to provide quality assessment. prior to presenting to the oncology units in the majority The topics investigated in the survey included preven- of the centres, notably in 19/21 institutions (90.5%) tive measures taken before and after admission to the before consultations, in 20/21 (95.2%) before day care hospital, instructions given to patients and professionals, outpatient infusion room admissions and in 20/20 general measures for risk reduction of virus spread, (100%) before overnight hospitalisation (figure 2). More specific measures in the hospitalisation unit, general specifically, the triage/screening tools used were phone organisation of the centre, organisation of multidisci- calls, interactive online platforms, nasopharyngeal or plinary meetings and activities of other healthcare profes- oropharyngeal swab tests, and/or chest CT scans. Phone sionals, staff management and antibody testing. The call was the most common sorting method, used in 17/21 survey was composed of 46 items, for which response (81%) institutions before outpatient consultations, in could be yes, no, not applicable or unknown. Addi- 18/21 (85.7%) before day care admissions and in 18/20 tional information was provided by comments, such as (90%) before hospitalisation. Less extensive use of the describing procedures used in particular situations. interactive online platform was noted: platforms were in The survey was completed by all the centres over a implementation in two centres, routinely used in 4/21 short time period in order to avoid bias from changing (19%) before consultations and day care unit admissions 2 Onesti CE, et al. ESMO Open 2020;5:e000853. doi:10.1136/esmoopen-2020-000853 Open access Figure 1 COVID-19 infection per 100 000 inhabitants. The curves represent the number of patients per 100 000 inhabitants with positive results for COVID-19 over time in the 10 countries included in the survey from 22 January to 13 May 2020. Each bar on the curves corresponds to one investigator. On the x-­axis, the timing from February to May is shown; on the y-­axis, the N of patients per 100 000 inhabitants is shown. and in 3/20 (15%) before hospitalisations. Swab test was Patients were educated in the majority of centres to not routinely performed for outpatients as it was used in take precautions in order to avoid virus transmission. In only 2/21 centres (9.5%). Its use was more common for particular, 20/21 (95.2%) centres educated patients to sorting patients in overnight wards, with 13/20 centres contact the medical oncology/haematology department (65%) using it routinely on unselected patients prior to if they developed symptoms potentially related to COVID- admission, with a result available within 12 hours in all the 19, and in 19/21 (90.5%) centres, patients were advised institutions. Chest CT scan was used in only one institu- to avoid visits to the unit in the presence of suspected tion (4.8%) as a screening method before surgery and symptoms. invasive procedures. A clinical check of symptoms was performed in the Allowance of visitors with patients hospital/clinic before entering the consultation room in Permission for family members and caregivers to accom- 17/21 centres (81%), before entering the day care unit pany patients was limited at this stage of pandemic in 20/21 (95.2%) and before hospitalisation in 19/20 spread, with only 8/21 (38.1%) centres allowing attend- (95%) units. ance to consultations, 4/21 (19%) to day care admissions and 8/20 (40%) to visit patients in overnight wards. Some exceptions were allowed: in 17/21 (81%) centres when a patient was unable to enter without assistance, in case of a new diagnosis of cancer in 3/21 (14.3%) centres, when bad news has to be announced in 4/21 (19%) centres and for terminally ill patients in 18/20 (90%) hospitalisation units. Some centres implemented virtual meetings with the family concomitantly to physical meetings with the patients. Protective equipment and disinfection In addition to social distancing and frequent hand washing/disinfection, some general measures were imple- mented to reduce risk of contagion (figure 3), such as the Figure 2 Triage/screening measures for COVID-19 in use of surgical masks for all patients in 19/21 (90.5%) oncological units. Triage (phone call and on-­line platform) institutions and for healthcare providers in all of the 21 and screening (swab test) measures taken before centres (100%), the use of non-­sterile gloves for physical consultation, day care admission and hospitalisation in 21 examinations in 12/21 (57.1%) and for nursing in 15/21 oncological units. (71.4%) centres. Filtering facepiece 2 and 3 masks were Onesti CE, et al. ESMO Open 2020;5:e000853. doi:10.1136/esmoopen-2020-000853 3 Open access Figure 3 General measure for risk reduction. Measures taken to reduce the risk of COVID-19 transmission in 21 oncological units. used in 1/21 (4.8%) institutions for non-­ aerosolising centres; palliative care admissions were reduced in 10/20 procedures, if no previous swab test had been done. (50%) centres; chemotherapy was transferred from over- Increased rates of disinfection process were also noted: night hospitalisation to day care unit in 5/20 (25%) of consultation rooms in 17/21 (81%) centres, of the day centres. In 10/21 (47.6%) centres, physicians discussed care units in 18/21 (85.7%) and of the hospitalisation the option to avoid intensive care in case of worsening units in 17/20 (85%) centres. of clinical conditions in those with terminal illness, regardless of COVID-19 infection, accepting the risk Reduction in physical contact of early death. In 13/20 (65%) centres, swab tests were To reduce contact (figure 3), physical examination was performed before hospitalisation, and in 10/20 (50%) abolished for asymptomatic patients in 16/21 (76.2%) centres, admissions were limited to COVID-19-­negative centres, and a targeted examination was preferred when necessary, for example, of the known sites of metas- patients. Two centres (10%) allow emergency admissions tasis or directed by symptoms. Blood pressure control without a negative test result. Retesting during hospital- was performed only when clinically indicated and not isation was done in only two centres (10%), weekly (one routinely in 19/21 (90.5%) institutions. Blood sampling centre) or biweekly (one centre). Nasopharyngeal or was reduced by at least 25% in 10/21 (47.6%) centres, oropharyngeal swab test for healthcare staff in the hospi- and the number of CT scans for evaluation of tumour talisation unit was done weekly by only one centre and response was reduced by at least 25% in 11/21 (52.4%) biweekly by another one, while 18/20 (90%) centres did institutions. The use of telemedicine was implemented in not do swab testing for healthcare professionals in the 16/21 (76.2%) centres. absence of symptoms. Several specific measures have been taken in inpa- In the majority of the hospitals, specific COVID-19 tient units to reduce patients’ stay and physical contacts units separate from non-­COVID units have been organ- (figure 4). Only private rooms were used in 7/20 (35%) ised (20/21 centres, 95.2%), and nurses and medical staff 4 Onesti CE, et al. ESMO Open 2020;5:e000853. doi:10.1136/esmoopen-2020-000853 Open access Figure 4 Specific measures in inpatient units. Measures taken to reduce the risk of COVID-19 transmission in 20 oncological hospitalisation units. in the oncology unit participate exclusively to COVID- 13/21 (61.9%) centres. Return to work for healthcare 19-­negative patients’ care in 12/21 (57.1%) centres. In professionals tested COVID-19-­positive was allowed after 20/21 (95.2%) centres, specific pathways for COVID- at least 7 days from diagnosis and 3 days without symptoms 19-­negative and COVID-19-­ positive/suspected patients in 5/21 cases (23.8%). In the remaining cases (16/21, have been organised. COVID-19-­confirmed or suspected 76.2%), a negative swab test was required. In particular, in cases at or during hospitalisation were transferred to the three centres, swab testing needed to be done after at least COVID-19 units in 18/20 (90%) centres. Specific sepa- 2 weeks of self-­isolation, and in three centres, two nega- rate day care units for COVID-19-­positive/suspected cases tive tests were required. In one (4.8%) centre, homework were established in 9/21 (42.9%) institutions, while in 1 was allowed for staff members older than 60 years, with (4.8%) case a specific room was used for these patients. serious comorbidity or with cohabitant family members At the start of the COVID-19 crisis, the oncology depart- with serious morbidity. ment, either in part or in full, moved to another location In addition to the previously discussed testing methods, in 4/21 (19%) centres, in the same hospital in three cases an emerging interest is the use of serology. During the and to another hospital in one case. survey period, this test was offered to healthcare workers Multidisciplinary meetings were done by videoconfer- in 8/21 (38.1%) centres, most frequently in the context of ences in 17/21 (81%) centres, while in 4/21 (19%) phys- a research project (7/21: 33.3%), and to patients in 9/21 ical meetings were still done respecting social distancing. (42.9%) centres, in four cases as clinical study (19%) and Multidisciplinary team members other than physician in five (23.8%) as routine practice. and nurses could still see patients in 10/21 (47.6%) centres, while in 16/21 (76.2%) centres, they managed all (10/21) or almost all (6/21) problems by phone or DISCUSSION videoscreen. The emergence of COVID-19 has caused a global health emergency, leading to multiple critical challenges. Not Management of staff suspected or confirmed as having only do clinicians and healthcare workers need to manage COVID-19 an extremely high load of very critically ill patients, but Self-­ isolation at home was the rule for staff members also they need to identify ways to reduce the risk of intr- presenting with fever in 20/21 (95.2%) centres and for ahospital contagion both among patients and health- staff members living with someone in self-­ isolation in care staff while using available resources as efficiently as Onesti CE, et al. ESMO Open 2020;5:e000853. doi:10.1136/esmoopen-2020-000853 5 Open access possible. This, however, has often resulted in a lack of and the risk of cross-­ reactivity with other coronavirus resources for routine patient care. strains.24–26 Chest CT scan seems to be more sensitive than In the oncology field, the initial response has been RT-­PCR for COVID-19 diagnosis and in 60%–93% of the focused on the protection of patients from the risk of infec- cases becomes positive before the RT-­PCR.25 27 However, tion. A shared approach, based on expert advice, includes the disadvantage of CT is the limited availability in terms limiting hospital access whenever possible, implementing of number of exams per day in each institution compared of a triage prior to admission to the hospital, reducing with the swab, which can be easily made on a large scale unnecessary consultations and exams, delaying follow-­up and is less cost-­effective. On the other hand, the result of visits, giving priority to adjuvant and curative treatment the swab test takes a longer time than CT scan. A potential over palliative ones, and avoiding advanced treatment solution to these concerns is the development of a rapid lines with low probability of clinical benefit.9 10 In this test, such as the serological test for IgA, IgM and IgG. context, the risk of jeopardising the effectiveness of Currently, its low sensitivity at the early phase of infec- cancer treatment and the risk of delayed diagnosis must tion, the delayed and the lower rate of seroconversion be taken into high consideration and should be carefully in patients with cancer and the inability to detect conta- analysed in future long-­term studies.18 giousness do not yet make it a suitable test to be used as a We conducted an observational study to analyse the diagnostic standard.28–30 Overall, at the moment, it seems activity of oncology centres located in the countries more appropriate to carry out a triage by telephone or most affected by the COVID-19 outbreak. These types of interactive platform before outpatient admissions and a studies are beneficial in order to identify best practices swab before hospitalisation. While the use of screening and to construct standardised algorithms for the preven- by means of a swab prior to hospitalisation is increasing, tion and management of this virus, and other emerging there was no unanimous agreement about retesting. A viruses, at long-­term. It is especially crucial in light of a single baseline test does not allow early detection of intra- likely secondary recrudescence of the infection outbreak. hospital infections and could miss paucisymptomatic or While for some aspects the applied procedures were presymptomatic patients.31 almost the same in all centres, others were quite different Another issue of concern is the implementation of a between centres, probably due to different burden of policy for return to work for healthcare professionals infection, differences in the availability of viral screening tested positive. While some centres require negative swab and resource availability. test, others do not, which may pose a risk of transmitting The use of personal protective equipment was one of the infection at the workplace, considering that a duration the cornerstones for prevention of virus spread that was of viral shedding up to 37 days has been described.32 33 almost unanimously accepted. Another interesting point Finally, predisposed dedicated facilities to manage is reducing the number of people accessing the hospital cancer care during COVID-19 pandemic could be advis- by limiting those accompanying or visiting patients. This able.34 Although COVID-19 wards have been organised second strategy is not currently used in all centres, due to in most centres, in only 57.1% of the centres healthcare the particular needs of patients with cancer. Therefore, a professionals caring for oncohaematological patients did limitation of the number of persons could be applied to not take part in the care of COVID-19-­positive patients. routine visits or access to the hospital during treatment, In conclusion, we analysed the prevention measures while exceptions can be made for heavily dependent taken in oncological units in high-­income countries in patients, when bad news has to be announced and for Europe and the USA, which effectiveness could be assessed terminally ill patients. in a later stage of the pandemic and in large observational The use of telemedicine reduces patient exposure to the studies. Although some recommendations for hospital hospital and is actually used in 76.2% of the institutions. management during the COVID-19 pandemic are actu- Although some legal and reimbursement issues remain, ally available, such as those of the European Centre for COVID-19 crisis has led to a rapid expansion of telemed- Disease Prevention and Control, our study allows assess- icine, which could remain a good option also outside the ment of adherence to this recommendation, in addition pandemic crisis, especially when a clinical examination is to providing an insight into the management of oncolog- not necessary and in areas of the world where reaching ical care during the pandemic in a real-­world context.8 the hospital raises practical difficulties for patients.21 Many procedures adopted, in fact, require agreement Almost all the oncological centres included in the survey at the international level. Some critical issues remain to performed a triage before admission to the hospital in be improved in order to increase the safety of treatment order to recognise symptoms early in suspected cases and for oncohaematological patients. The same level of care to avoid contamination of other patients and healthcare should be extended to the entire healthcare system, to professionals. Triage is supplemented with diagnostic less well-­supplied centres and to low-­income countries. tests, usually swab, with nasal sampling resulting more efficiently than throat sampling.22 23 The main issue with Author affiliations this tool is the relatively low sensitivity of about 70%, the 1 Department of Medical Oncology, CHU de Liège, Liege, Belgium multiplicity of primers that can be used to perform the 2 Laboratory of Human Genetics, GIGA Research Institute and University of Liège, reverse-­transcriptase polymerase chain reaction (RT-­PCR) Liège, Belgium 6 Onesti CE, et al. ESMO Open 2020;5:e000853. doi:10.1136/esmoopen-2020-000853 Open access 3 Department of Medicine and Division of Oncology, University of California San MedSIR. SAH reported grants from Ambrx, Amgen, Arvinas, Bayer, Daiichi-­Sankyo, Francisco, Comprehensive Cancer Center, San Francisco, California, USA Genentech/Roche, GSK, Immunomedics, Eli-­Lilly, Macrogenics, Novartis, Pfizer, 4 UO Patologia Mammaria e Ricerca Traslazionale, Breast Unit, Azienda Socio OBI Pharma, Pieris, Puma, Radius, Sanofi, Seattle Genetics and Dignitana; travel Sanitaria Territoriale di Cremona, Cremona, Italy fees from Lilly and Novartis; stock options from NK Max; editorial support from 5 University of Trieste, Trieste, Italy Roche/Genetech, Eli-­Lilly and Pfizer. MT declares travel, accomodations, expenses 6 Oncology Department, University Hospital Antwerp (UZA), Antwerp, Belgium by Roche, Bristol-­Myers Squibb, Astra Zeneca, Takeda; activity as medical writer 7 Oncology Department, CHUV - Centre Hospitalier Universitaire Vaudois, Lausanne, supported by Novartis and Amgen, outside the present work. MC reported funding Switzerland to the institution from Sanofi, Pierre-­Fabre, AstraZeneca, Servier, Novartis, Abbvie, 8 Department of General Medical Oncology, University Hospitals Leuven, Leuven, Accord and Pfizer; personal fees from GT1, Sanofi, Pierre-­Fabre, AstraZeneca, Belgium Servier, Novartis, Abbvie, Accord and Pfizer. RB reported personal fees from Accord, 9 AstraZeneca, Daiichi-­Sankyo, Eisai, Eli-­Lilly, MSD, Novartis, Roche, Puma, Pierre-­ Breast Center, Dept. OB&GYN and CCLMU, Ludwig Maximilians University Hospital, Fabre and Sandoz; grants from Daiichi-­Sankyo, Novartis and Roche; non-­financial Munich, Germany 10 support from Eli-­Lilly and MSD. SDP reported personal fees from Roche, Novartis, Departamento de Medicina, Instituto de Investigación Sanitaria Gregorio Marañón, Pfizer, Celgene, AstraZeneca and Eli-­Lilly. VM reported funding to the institution Universidad Complutense de Madrid, Madrid, Spain 11 from Novartis, Roche, Seattle Genetics and Genentech; personal fees from Amgen, Feinberg School of Medicine, Northwestern University, Robert H. Lurie AstraZeneca, Daiichi-­Sankyo, Eisai, Pfizer, MSD, Novartis, Roche, Teva and Seattle Comprehensive Cancer Center, Chicago, Illinois, USA Genetics; consultancy honoraria from Genomic Health, Hexal, Roche, Pierre-­Fabre, 12 Oncology Department, Vall d’Hebron Institute of Oncology (VHIO), Barcelona, Spain Amgen, ClinSol, Novartis, MSD, Daiichi-­Sankyo, Eisai, Eli-­Lilly, Tesaro, Seattle 13 IOB Institute of Oncology, Madrid, Spain Genetics and Nektar. J-­PM reported personal fees from Roche, AstraZeneca, Bayer, 14 Medical Oncology Department, Maastricht University Medical Center (MUMC), Innate, Merck-­Serono, Boeringher, BMS, Novartis, Janssen, Incyte, Cue Biopharma, Maastricht, The Netherlands ALX Oncology and Pfizer; grant from BMS; travel fee from Amgen; other support 15 Los Angeles/Jonsson Comprehensive Cancer Center, University of California Los from MSD, Psioxus, Debio and Nanobiotix. GJ reported personal fees from Novartis, Angeles, Los Angeles, California, USA Roche, Pfizer, Eli-­Lilly, Amgen, BMS, AstraZeneca, Daiichi-­Sankyo and Abbvie; 16 Hemato-­Oncology Department, Centre Hospitalier de Luxembourg, Luxembourg, grants from Novartis, Roche and Pfizer; non-­financial support from Medimmune Luxembourg and Merck KGaA. 17 Medical Oncology 2, Ospedale Policlinico San Martino, Genova, Italy Patient consent for publication Not required. 18 Institut de Cancérologie de l’Ouest, Centre René Gauducheau, Saint Herblain, France Provenance and peer review Not commissioned; externally peer reviewed. 19 Department of Medicine I, Medical University of Vienna, Vienna, Austria Data availability statement Data are available upon reasonable request. 20 Dipartimento di Medicina Clinica e Chirurgia, Università degli Studi di Napoli Open access This is an open access article distributed in accordance with the Federico II, Napoli, Italy 21 Creative Commons Attribution Non Commercial (CC BY-­NC 4.0) license, which Department of Medical Oncology, Centro di Riferimento Oncologico, Aviano, Italy permits others to distribute, remix, adapt, build upon this work non-­commercially, 22 Medical Oncology Department, UZ Gent, Gent, Belgium and license their derivative works on different terms, provided the original work is 23 Ginecology Department, University Medical Center Hamburg-­Eppendorf, Hamburg, properly cited, any changes made are indicated, and the use is non-­commercial. Germany See: http://​creativecommons.​org/​licenses/​by-​nc/​4.​0/. 24 Medical Oncology Department, Breast Center of Eastern Switzerland, St Gallen, Switzerland ORCID iDs 25 Oncology Department, Cliniques Universitaires St. Luc, Brussels, Belgium Concetta Elisa Onesti http://​orcid.​org/​0000-​0002-​8360-​5026 26 Istituto Oncologico Veneto Istituto di Ricovero e Cura a Carattere Scientifico, Marc Peeters http://​orcid.​org/​0000-​0003-​4969-​2303 Padova, Italy Marco Tagliamento http://​orcid.​org/​0000-​0001-​7461-​023X 27 Division of Medical Oncology, University of Padova, Padova, Italy Fabio Puglisi http://​orcid.​org/​0000-​0003-​0573-​4938 28 Medical Oncology Department, Institut Jules Bordet, Bruxelles, Belgium 29 Medical Oncology Department, Université Libre de Bruxelles, Bruxelles, Belgium 30 Université de Liège, Liege, Belgium Twitter Fabio Puglisi @Fabio Puglisi REFERENCES 1 Zhu N, Zhang D, Wang W, et al. 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