Critical Reviews in Oncology / Hematology 150 (2020) 102972

Contents lists available at ScienceDirect

Critical Reviews in Oncology / Hematology

journal homepage: www.elsevier.com/locate/critrevonc

Cancer patients and research during COVID-19 pandemic: A systematic T

review of current evidence
Elissar Moujaess, Hampig Raphael Kourie*, Marwan Ghosn
Hematology-Oncology Department, Faculty of Medicine, Saint Joseph University of Beirut, Lebanon

A R T I C LE I N FO A B S T R A C T

Keywords: The novel coronavirus, also known as SARS-Cov-2 or COVID-19 has become a worldwide threat and the major
COVID-19 healthcare concern of the year 2020. Cancer research was directly affected by the emerging of this disease.
Systematic review According to some Chinese studies, cancer patients are more vulnerable to COVID-19 complications. This ob-
Cancer patients servation led many oncologists to change their daily practice in cancer care, without solid evidence and re-
Research
commendations. Moreover, the COVID-19 manifestations as well as its diagnosis are particular in this special
Oncology
population. In this review paper we expose the challenges of cancer management in the era of SARS-CoV-2, the
epidemiological, clinical, pathological and radiological characteristics of the disease in cancer patients and its
outcomes on this population. Finally, we focus on strategies that are followed in cancer management with review
of national and international guidelines.

1. Introduction to protect this vulnerable population from the virus exposure as well as
from the disease progression resulting from testing and treatment de-
The novel coronavirus, also known as SARS-Cov-2 or COVID-19 has lays. In this article, epidemiological, radiological and clinical features
become a worldwide threat and healthcare concern. Human to human of adult cancer patients with COVID-19 will be reviewed based on an
transmission of the virus occurs through respiratory droplets (by extensive review of the literature, as well as diagnostic and therapeutic
coughing or sneezing) and through direct contact with an infected pa- strategies suggested by healthcare providers and institutions in en-
tient or indirect contact with fomites in his environment (Li et al., demics areas, particularly China and Italy.
2020a; Ong et al., 2020). Since its outbreak in China at the end of 2019
and until the 5th of April 2020, the pandemic has affected more than a 2. Materials and methods
million of people and caused 62,773 deaths globally (20200405-sitrep-
76-covid-19.pdf, 2020). It is thought that patients with comorbid con- In order to review the particularities of COVID-19 in adult patients
ditions are more susceptible to manifest complications of the viral in- with cancer, an extensive electronic search of the literature was con-
fection (Guan et al., 2020a). According to a recently published Chinese ducted in the PubMed database until the 5th of April 2020. The fol-
cohort, patients with cancer had a higher risk of developing severe lowing keywords with Boolean operators were used ‘covid-19’, 'novel
events (intensive care unit admission, invasive ventilation, or death) coronavirus’ and ‘SARS-CoV-2' in combination with ‘cancer’, 'neo-
compared with patients without cancer (39 % vs 8%, p = 0·0003) plasm’, 'oncology’ and ‘malignancy’. A total of 223 articles were ex-
(Liang et al., 2020). Moreover, public health measures that are im- tracted. We included articles in English as well as articles in French
plemented in order to control the disease spread aim to decrease pre- because we are familiar with this language. Abstracts in English of ar-
ventable hospital admissions and elective procedures (Cao et al., 2020). ticles in Chinese language were also included. Duplicated articles and
However, cancer patients need continuous care, and undergoing diag- articles that were published before the era of SARS-Cov-2 (i.e., before
nostic tests or therapeutic interventions is not a luxury, whereas their December 2019) were excluded. Titles and abstracts of retrieved arti-
potential COVID-19 exposure could be very risky, or even fatal. Re- cles were screened for eligibility, and then entire texts were analyzed
markable efforts are made to understand the particularity of cancer and 88 papers that respond to our objectives were included in this re-
patients who contract the novel coronavirus, to overcome the diag- view. Our work is summarized in the PRISMA diagram below (Fig. 1).
nostic and therapeutic challenges and to implement recommendations

⁎
Corresponding author.
E-mail address: [email protected] (H.R. Kourie).

https://doi.org/10.1016/j.critrevonc.2020.102972
Received 13 April 2020; Accepted 16 April 2020
1040-8428/ © 2020 Elsevier B.V. All rights reserved.
E. Moujaess, et al. Critical Reviews in Oncology / Hematology 150 (2020) 102972

Fig. 1. PRISMA flow chart of article selection process.

3. Results
MulƟple
Out of 88 articles, six were in French language and 19 were in Others 8%
6%
Chinese language with English abstracts. Most of the papers consisted of
United Kingdom
short editorials, letters, correspondence or comments. Ten Cohort stu- 6%
dies were identified (retrospective, prospective or cross-sectional ana- China
France
42%
8%
lysis) as well as 9 case reports and one case series. Only four of the
cohort studies exclusively included cancer patients. Of note, all cohort
studies were conducted in China. Most of the reported cases originated Unites States of Italy
from China and Italy. America 17%
13%
59 % of the published papers originated from China and Italy (52 of
88). Seven works were multinational and the majority of them were
multicontinental, issued in collaboration between researchers from Fig. 2. The percentage of contribution of different countries in the published
articles on COVID-19 and cancer.
Asia, Europe and the Americas. We identified one article originating
from each of the following countries: Canada, India, Singapore, Spain
and Saudi Arabia. The pie chart below (Fig. 2) shows the distribution of • Strategies for risk reduction and management of cancer patients
the articles included in our review according to the country of origin. during COVID-19 outbreaks (57 articles).
Researchers in oncology are preoccupied by more than one aspect of
the COVID-19. Subjects of interest in the papers that were included in Many expert recommendations on the diagnosis and treatment of
this review could be divided in four categories: cancer patients during the novel coronavirus outbreak were formulated
so far. Designs and strategies that focused on gastrointestinal and lung
• Cancer research in the era of COVID-19, and the effect of cancer tumors were the most prevalent, followed by urogenital neoplasms and
breast and other gynecological malignancies. The management of he-
therapy on COVID-19 patients (6 articles).
• Epidemiological, clinical, pathological and radiographic features of matological cancers was also discussed in three papers. Until the end of
March, no universal guidelines were adopted. However, the first week
cancer patients with COVID-19 (14 articles).
• Outcomes of cancer patients with a SARS-CoV-2 infection (11 arti- of April was marked by the emergence of consensus guidelines and
propositions from multiple national and international groups.
cles).

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Fig. 3. Number of publications on cancer and COVID-19 per week between the 10th of February and the 4th of April 2020.

Fig. 3 shows the number of published articles per week that are patient whose prognosis and wellbeing is dependent on an investiga-
interested in cancer and COVID-19 between the 10th of February and tional treatment and a protocol to which he is adhering. Second one is
the 4th of April 2020. making an effort to flatten the curve of COVID-19 infection by mini-
This article will discuss the various aspects of COVID-19 in cancer mizing any unnecessary exposure to a suspicious environment. Finally
patients assessed in the literature. they emphasize on psychosocial support of the patient and of the re-
search team in the middle of the outbreak (Shuman and Pentz, 2020).
3.1. Cancer research in the era of COVID-19
3.2. Epidemiological, clinical, pathological and radiographic features of
With the declaration of COVID-19 pandemic, strict public health cancer patients with COVID-19
measures were recommended by authorities to limit the virus spread.
Those measures also apply to cancer research centers that found their At the beginning of the epidemic in China, multiple epidemiological
activity declining due to quarantining measure, working in shifts and studies were conducted to evaluate characteristics of patients with
lacking supplies. Thus, researchers faced the necessity to make deci- COVID-19. Some of these studies included a subgroup of cancer pa-
sions on continuing or interrupting trials (COVID-19 Challenges Basic tients. For instance, Wei-Gie Guan et al. analyzed data of 1099 patients
Researchers, 2020). While experimental researches are crucial for with laboratory-confirmed COVID-19 through January 29, 2020. They
providing the best care for cancer patients, many centers are trying to identified in their cohort 261 patients (23.7 %) with comorbidity. Only
make changes to their programs and adapt to the new situation without 10 of these patients had a history of cancer (0.9 % of all patients). 3 of
interrupting their activity. Moreover, high authorities such as the FDA these 10 patients had a severe presentation on admission while the
issued guidelines that recommend being more flexible about protocols. others had mild symptoms (Guan et al., 2020b). Another Chinese ret-
Some measure were taken from remoting communication with patients rospective cohort studied 69 cases of COVID-19 in Wuhan. Disease se-
for follow up, making changes and exceptions to trials protocols to verity at presentation was assessed by the SpO2 as the sole criteria, with
reducing multiple hospital visits and routine follow up, postponing new a cutoff of 90 %. Among these 69 patients, four had a history of ma-
clinical trials, etc. (Clinical Research Slows as COVID-19 Surges, 2020). lignancy of whom only one patient presented with an SpO2 < 90 %
On the other hand, some cancer research laboratories opted for (Wang et al., 2020a).
pivoting their experiments in anti-neoplastic agents towards exploring In both cohorts previously cited the number of patients who had a
therapeutic options for COVID-19 infection. For instance, Chinese trials severe presentation was higher than that of less severe cases, but this
are assessing the role of the anti-VEGF bevacizumab, the myeloma drug observation did not apply to the sub-group of patients with malignancy.
thalidomide, the PD-1 inhibitor camrelizumab and other anti-cancer However, these data are not enough to conclude that cancer patients
agents in the treatment of SARS-CoV-2 infections. The potential benefit tend to present with milder symptoms than the rest of the population.
of other targeted therapies such as afatinib, carfilzomib and ixazomib Liang et al. were the first to publish data regarding cancer patients
was highlighted in the literature (Cancer Labs Pivot to Battle COVID-19, who are diagnosed with COVID-19. Their Chinese cohort was the lar-
2020). gest and the only prospective cohort to date interested in oncology
Many other cancer drugs are being investigated in this field. For patients. It included 1590 COVID-19 cases of whom 18 (1 %; 95 % CI
example, a theoretical role of kinase inhibitors in the reduction of in- 0·61–1·65) had a history of cancer. This was higher than the incidence
fectivity of well-known viruses such as Ebola and Hepatitis C is de- of cancer in the overall Chinese population (0·29 %). The most frequent
scribed, suggesting that drugs like sunitinib and erlotinib would po- primary tumor was lung cancer. Four of 16 patients had received che-
tentially be effective against SARS-CoV-2 (Stebbing et al., 2020). motherapy or surgery within the prior month, and twelve were in re-
Moreover, a group of researchers used network proximity analyses mission at the time of the infection. The mean age was 63·1 years in
of drug targets and virus–host interactions in the human interactome to cancer patients vs 48·7 years in non-cancer patients. There was no dif-
identify repurposable drugs and potential drug combinations for the ference in gender between the two groups. Clinical presentation was
treatment of SARS-CoV-2. Three combinations were deemed effective: marked by more polypnea in the cancer group (47 % vs 23 %), and
sirolimus plus dactinomycin, mercaptopurine plus melatonin, and tor- imaging findings by more severe CT scan at baseline (94 % vs 71 %),
emifene plus emodin, all of which consisting of at least one anti–cancer without significant difference in severity on chest X-ray (Liang et al.,
agent (an immunosuppressant, an antineoplastic agent and a selective 2020).
estrogen receptor modulator respectively) (Zhou et al., 2020). These data were helpful in clarifying epidemiologic and clinical
Amidst this rapid evolution of the COVID-19 should be kept in mind features of cancer patients during the COVID-19 pandemic, but were
the need to respect some clinical research ethics. In fact, the medical criticized by Wang et al: the higher incidence of cancer in this cohort
ethics editorial team of The Oncologist focused on three crucial con- compared to that of cancer in the general Chinese population was in-
siderations in cancer research. First one is non-abandonment of a terpreted as an increased risk for cancer patients to be infected with the

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COVID-19. However, only four of the 18 patients had a disease that is present at the time of surgery (Tian et al., 2020).
actively treated while twelve were in complete remission and two had • Some clinical and biological features can mask a COVID-19 pre-
an unknown treatment status. Therefore their infection might be related sentation in cancer patients. This is the case of hematologic malig-
to another etiology than their cancer (Wang and Zhang, 2020). nancies where laboratory results can be misleading. For instance, a
After Liang et al., two other cohorts (one cross-sectional and one Chinese patient with a history of non-Hodgkin lymphoma and CLL
retrospective) were conducted during the same time frame in China. treated with chlorambucil presented with signs of disease progres-
Jing et al. (Yu et al., 2020a) published a cross-sectional analysis of 1524 sion as well as respiratory symptoms. She initially denied any ex-
patients with cancer in a tertiary hospital in the city of Wuhan. 12 of posure to a confirmed case, and the diagnosis of COVID-19 was
these patients (0.79 %) were diagnosed with COVID-19 pneumonia. delayed because of the high white blood counts count (91·85 × 109
They concluded that the infection rate of COVID-19 in cancer patients cells/L) and the focus on the treatment of his underlying malignancy
was higher than the cumulative incidence reported over the same (Jin et al., 2020).
period in Wuhan (0.79 % vs 0.37 %, OR 2.31 [95 % CI, 1.89–3.02]).
Zhang et al. retrospectively analyzed 28 COVID-19-infected cancer 3.3. Outcomes of cancer patients with a SARS-CoV-2 infection
patients (Zhang et al., 2020a). Of note, the median age of infected
patients was similar in both studies (66 and 65 years respectively), and Few studies that analyze the impact of a SARS-CoV-2 infection on
lung cancer was also the most predominant type with more than half of patients with malignancy were found in our literature review. However,
the patients (seven of 12 patients) in the first cohort and 25 % (7 of 28) we can make some conclusions from cohort studies that included cancer
in the second one. These conclusions were compatible with those of the patients.
prospective cohort of Liang et al. Moreover, both studies implied that A study performed on 24 critically ill patients in Seattle found that
hospital admission was an independent risk factor to acquire a SARS- most of these patients had comorbid conditions, however a history of
CoV-2 infection, because most of cancer patients in the first study were cancer was not found in any of these patients (Bhatraju et al., 2020). We
receiving active in-hospital treatments (chemotherapy with or without know that this is a very small sample, but we still can tell that patients
immunotherapy, radiotherapy or surgery), and 8 of 28 patients (28.6 who have other underlying chronic conditions such as asthma or dia-
%) in the second study were suspected to have a hospital-associated betes might be more concerned about becoming critically ill if infected
transmission. with the SARS-CoV-2 than cancer patients.
Not only clinical presentation of COVID-19 in patients with cancer is An analysis of the first 1975 COVID-19 patients in China was per-
particular, but also diagnosing this disease is challenging due to mul- formed, and the first 17 deaths were reviewed. Most of the cases who
tiple factors: died were elderly patients (median age 75; range 48‐89 years) and had
comorbidities or a history of recent surgery. Of the 17 deaths, only one
• Cancer patients might have atypical radiographic features. Qu et al. patient had a history of cancer. He was an 86-year-old man with a
reported the case of one patient with lung adenocarcinoma who had history of colon cancer and underwent a colon cancer surgery (Wang
a laboratory confirmed COVID-19 infection with diffuse, irregular, et al., 2020b). Of course, this small sample prevents us from extra-
small ground-glass opacities with partial consolidation on day 10 of polating these data; however, this patient had other comorbid condi-
infection on chest CT-scan. This is not compatible with the typical tions (hypertension and diabetes mellitus) that, along with his age and
peripheral subpleural ground-glass infiltrates (Qu et al., 2020). male gender make him more vulnerable to a SARS-CoV-2 infection. In
• Cancer patients might have radiographic findings similar to those of fact, a nationwide analysis of 1590 COVID-19 hospitalized patients in
a SAR-CoV-2 infection and can be misleading. A Chinese article 575 Chinese hospitals between December 11th, 2019 and January 31 st,
reported the cases of five of 139 cancer patients who had ground- 2020 showed that the most prevalent comorbidities were hypertension
glass opacities on baseline chest CT-scans. Three of these patients (16.9 %) and diabetes (8.2 %). Only 18 patients (1.1 %) had a history
underwent RT-PCR, had a negative test and were considered nega- on malignancy. However, severe cases in this analysis were more likely
tive for COVID-19. The most retained diagnosis in these patients was to have a malignancy (50.0 % versus 15.6 %) compared with non-severe
another viral infection (Zhu et al., 2020). Nevertheless, many cases. The composite endpoints consisting of admission to intensive
sources now admit that radiographic findings are more sensitive care unit, or invasive ventilation, or death were also analyzed, and after
than RT-PCR in detecting COVID-19 (Fang et al., 2020) and the adjustment for age and smoking status a history of malignancy was the
previously reported cases could have a COVID-19 infection that was fourth most common risk factor of reaching the composite endpoints
missed because of a false negative PCR test. with a HR of 3.50 (95 %CI 1.60–7.64) (Guan et al., 2020a). On the
• Due to the high frequency of routine chest imaging in the follow up other hand, in the 1099 patients cohort of Wei-Gie Guan et al. pre-
of cancer patients, incidental findings suggestive of COVID-19 may viously mentioned, out of 10 patients who had cancer only one patient
not be infrequent. These findings are a source of frustration for the experienced an adverse event (ICU admission, ventilation or death)
patient and the physician, as they may suggest either another dif- (Guan et al., 2020b). This may suggest that adverse outcomes in ma-
ferential diagnosis or a COVID-19 infection at an early asympto- lignancy are not as frequent as we think. Moreover, an analysis of 85
matic stage especially in regions of high disease prevalence as was fatal cases of COVID-19 in China showed that 58 had comorbidities, of
the case of an Italian patient who was referred for an FDG-PET/CT whom 7% had a cancer history while 60 % had hypertension or dia-
(Polverari et al., 2020). This was then highlighted by an Italian betes mellitus (Du et al., 2020).
analysis performed in a nuclear medicine center where incidental We believe that these results should be interpreted with caution in
findings were recorded in 7 of 65 asymptomatic patients who un- the absence of adjustment to the prevalence of the different co-
derwent imaging studies, of whom 5 had a laboratory confirmed morbidities in the Chinese population.
infection (Albano et al., 2020). The nationwide cohort of Liang et al. previously described, speci-
• Due to similarity in symptoms between the infection and the un- fically targeting cancer patients, concluded that this population was
derlying disease, especially in lung cancer patients and patients with predisposed to higher risk of severe events (ICU admission, mechanical
pulmonary metastasis, the diagnosis of COVID-19 may be delayed. ventilation or death) compared to non-cancer patients (39 vs 8%; p =
In two patients who were programmed for elective lobectomy for 0.0003), and that among cancer patients, those with a recent history of
early stage lung cancer in China, a retrospective diagnosis of SARS- chemotherapy or surgery had a higher risk of severe events than those
CoV-2 was made after patients worsened their symptoms post-op- who did not receive treatment (Liang et al., 2020). These data should
eratively. The examination of pulmonary pathology showed that also be carefully interpreted, not only because of the small sample, but
inflammatory changes consistent with interstitial disease were also because cancer patients in this cohort had a significantly older

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median age than their control (63·1 vs 48·7 years) as well as a more patients’ safety. These measures consist of prioritizing laparoscopic
significant history of smoking, suggesting that these two factors might procedures in cancer surgery to minimize the exposure to aerosolized
be more associated with worse COVID-19 outcomes than the cancer specimen (Kimmig et al., 2020) and limiting endoscopic diagnostic
history itself (Wang and Zhang, 2020). procedures to the necessary with application of strict protective mea-
Conversely, in the Jing et al. cohort, outcome of cancer patients was sures particularly in bronchoscopy (Ost, 2020). Some medical and
a secondary endpoint, but authors could conclude that three of 12 pa- imaging oncology wards were completely re-organized to safely ac-
tients (25.0 %) developed SARS; 1 patient required an ICU admission commodate cancer patients (Ngoi et al., 2020; Jazieh et al., 2020;
and 3 deaths (25.0 %) were recorded (Yu et al., 2020a). Zhang et al. Czernin et al., 2020).
reported a higher rate of adverse events (53.6 %) and mortality (28.6
%) in their 28 cancer patients cohort, with a higher risk of sever events 3.4.1. The Chinese experience
in patients who had their last anti-tumor treatment within 14 days of Since the outbreak of SARS-CoV-2 in China, the whole healthcare
the infection (HR = 4.079, 95 %CI 1.086–15.322, P = 0.037) (Zhang system was shifted towards the management of SARS-CoV-2 patients.
et al., 2020a). Chinese oncologist faced difficulties in providing the best care for their
The three above studies (Liang et al., 2020; Yu et al., 2020a; Zhang patients. We add to this that integrative cancer therapy that involves
et al., 2020a) encouraged physicians to withhold or postpone cancer close contact of the care provider with patients is widely available in
treatment during the epidemic, and this need was mainly urged by China and constitutes a great risk during the pandemic (Yang et al.,
Liang et al. based on an increased risk of adverse events in patients that 2020a). As of the 1st of February, almost a month following the de-
received chemotherapy or underwent recent surgery prior to the in- claration of the epidemic, more than a dozen of articles that propose
fection, predisposing them to hematological toxicity and to an im- management strategies for oncology patients were published. Most of
munocompromised state. these articles have their bodies in Chinese. Abstracts of these articles
Regarding patients treated with immunotherapy, no clear data are were reviewed to form a picture of the oncology practice in China
yet available. A case report appeared on the 27th of March discussing during the COVID-19 pandemic. Common to all works was the en-
the history of an Italian patient with metastatic lung cancer who has couragement of a multidisciplinary approach and the delay of every
been treated with nivolumab in the second line for 7 years with an elective procedure. However, the definition of elective procedures is
excellent response, but died of a COVID-19 infection after a rapid not universal (Wang et al., 2020c).
clinical deterioration (Bonomi et al., 2020). Nevertheless, according to Most of the Chinese literature emphasized on gastrointestinal tu-
an Italian researcher, the conclusions of Liang et al. should be carefully mors, especially the surgical management (Yu et al., 2020b; Ma et al.,
extrapolated to patients receiving immunotherapy, especially in the 2020; Li et al., 2020b; Hu et al., 2020a). A COVID-19 positive patient
adjuvant setting or for a curative intent, although the similarity in the with early stage colon cancer was successfully treated with colectomy
mechanism of action of immune-checkpoint inhibitors and the COVID- without complications after receiving anti-viral therapy and negating
19 infection in terms of cytokine release, and the common radiological his RT-PCR on two occasions (Ye et al., 2020). Since fecal-oral trans-
finding of immunotherapy-induced pneumonitis and COVID-19 infec- mission cannot be excluded to date, experts encourage laparoscopic
tion make this issue more challenging (Bersanelli, 2020). techniques (Yu et al., 2020b), prioritizing non-surgical and interven-
Moreover, no patients in the prospective Chinese cohort were tional management such as stent placement for gastro-intestinal ob-
treated with targeted therapy, and only one patient was on osimertinib struction, avoiding endoscopic procedures (Chen and Peng, 2020; Hu
in the cohort of Jing et al. In the absence of data, the safety of targeted et al., 2020b; Luo and Zhong, 2020), providing isolation areas for in-
therapy is still unknown, but according to a case reported in China, one vasive interventions for suspected or confirmed cases (Chen and Peng,
patient with EGFR positive lung adenocarcinoma treated with osi- 2020; Luo and Zhong, 2020). As for the medical management, a group
mertinib was diagnosed with COVID-19 and successfully treated with of experts suggested maintaining chemotherapy for metastatic patients,
the antiretroviral lopinavir/ritonavir, without withholding treatment providing necessary treatment for patients who have a progressive
with osimertinib. No adverse outcomes were recorded (Zhang et al., disease and decreasing intensity and frequency of adjuvant che-
2020b). motherapy (Li et al., 2020). Chinese physicians adopted modifications
This said, some authors suggest that because no solid evidence exists not only in the therapeutic strategies but also in the diagnostic proce-
yet, treatment modification or interruption should not be a standard dures of cancer patients (Wu et al., 2020; Zhang and Xu, 2020). De-
and should be individualized and discussed with every patient (Shankar laying gastro-intestinal diagnostic procedures for patients with a stable
et al., 2020). disease was recommended by a group of practitioners (Luo and Zhong,
2020).
3.4. Strategies for risk reduction and management of cancer patients during As for lung cancer, keeping a high index of suspicion for a COVID-19
COVID-19 outbreaks infection and protecting vulnerable patients are priorities (Li et al.,
2020c; Xu et al., 2020; Yang et al., 2020b), as three Chinese cohorts
While every cancer patient and his healthcare provider are con- demonstrated that lung cancer is the most type of cancer susceptible to
cerned about the risk of transmission of COVID-19 in hospital settings, COVID-19 infection. Guidelines are directed toward maximizing out-
the risk of disease progression with treatment delay started to become patient follow-up and treatment, delaying possible therapies and pro-
more serious with the pandemic persisting (Burki, 2020a; Extance, cedures, screening patients for COVID-19 infection even with a low
2020; Kutikov et al., 2020; The Lancet Oncology null, 2020), and the index of suspicion due to similarities of symptoms with those of the
healthcare system distraction towards COVID-19 might have harmful underlying cancer of the treatment's adverse events (Zhao et al., 2020;
consequences on cancer patients (Cortiula et al., 2020). The urgent Lung Cancer Study Group et al., 2020).
need for guidelines implementation to protect cancer patients from Furthermore, outpatient care for breast cancer patients was also
acquiring a COVID-19 without harming them is discussed by many highlighted in one article (Liu et al., 2020). Another small Chinese
authors in the literature. In the absence of universal guidelines, most of study identified the lack of strict guides for the management of gyne-
the strategies adopted involve prioritizing urgent situations such as cological cancer in an endemic region (Zhang et al., 2020c).
acute leukemia, curative treatments for aggressive diseases, and ad- This said, China obviously witness a change in practice in the
juvant and neoadjuvant therapies while withholding or postponing management of oncology patients during the COVID-19 pandemic.
palliative therapies for poor prognosis patients (Hanna et al., 2020).
Telemedicine is also encouraged (Connor et al., 2020). Measures to 3.4.2. The Italian experience
protect medical staff are proposed because this indirectly impacts After China, Italy was one of the first countries that experienced a

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tragic increase in the incidence and mortality rate of COVID-19 cases, 3.4.3. The French experience
with more than 100,000 cases and up to 11,600 deaths by the end of Practice of oncology in France was not different than that in China
March 2020 (20200331-sitrep-71-covid-19.pdf, 2020). Italy rapidly and Italy, but some French societies have recently issued formal
complained of a shortage of resources and some oncologists were called guidelines for the management of specific types of malignancy. All
to help in the fight of COVID-19, some hospitals were transformed to these propositions meet the recommendations published on the 14th of
admit COVID-19 patients only. An Italian young oncologists group March by a group of French experts solicited by the president of Public
suggested some measures to adapt to the situation based on their cur- Health Council on SARS-CoV-2 infection and solid cancers (You et al.,
rent practice. Those measures consisted mainly of delaying some an- 2020; Grellety et al., 2020).
ticancer treatment on case-by-case evaluation of the risk/benefit ratio We here summarize some of these guidelines:
especially for second line treatments and beyond for incurable meta-
static disease, maintaining adjuvant and neoadjuvant as well as first • In breast cancer, the Collège Nationale des Gynécologues et
line metastatic treatment, delaying imaging assessment for clinically Obstétriciens Français (CNGOF), the Société d’Imagerie de la
stable patients, encouraging remote follow-up except for patients with FEMme (SIFEM), the Société Française de Chirurgie Oncologique
clinical complaints suggestive of disease progression or for those who (SFCO), the Société Française de Sénologie et Pathologie Mammaire
insist to get a physical exam, limiting caregivers company and re- (SFSPM) and the French Breast Cancer Intergroup-UNICANCER
specting personal protection and distancing measures (Lambertini (UCBG) recommend to withhold screening programs during the
et al., 2020). pandemic, investigate only BIRADS IV and above lesions, perform
Similarly, remote monitoring and home care were encouraged ambulatory surgeries and avoid complicated reconstruction sur-
(Mussetti et al., 2020). A group of practitioners in Tuscany, Italy, geries, avoid surgery in COVID-19 positive patients who have low
adopted and validated a home care protocol that consisted of a double grade tumors, delay adjuvant radiotherapy and privilege hypo
triage to protect patients with cancer. The first triage aims to screen fractionated protocols, maintain palliative radiotherapy for meta-
patients and their cohabiters for any sign or symptom of a COVID-19 static disease in patients with good performance status, maintain
infection via a telephone interview, while a second telephone interview neoadjuvant and adjuvant chemotherapy but opt for the shortest
aims to schedule home access with variable frequency of visits based on possible protocols and prioritize oral chemotherapy in the meta-
symptoms burden and patient’s prognosis (Porzio et al., 2020). static setting (Gligorov et al., 2020).
One article in the Italian literature highlighted the lack of re- • In gynecological cancer, the FRANCOGYN group for the CNGOF
commendations that guide the diagnosis, follow-up and treatment of propose recommendations that do not differ much from the standard
patients with head and neck cancer in the era of SARS-CoV-2 (De Felice of care, except that they emphasize on radio-chemotherapy in the
et al., 2020). As for lung cancer, practical suggestions appeared on the first line setting for cervical cancer instead of surgical treatment,
27th of March in the ESMO Open to guide physicians in making deci- and on the neoadjuvant chemotherapy for advanced ovarian cancer
sions on which treatment and procedure to prioritize (Banna et al., even for tumors that are judged to be resectable in order to reduce
2020). high risk surgeries and long ICU stays (Akladios et al., 2020). Note
Most of the other Italian published works targeted urological and that similar suggestions were proposed by a multinational group of
gastrointestinal tumors, also with more focus on the surgical aspect practitioners (Ramirez et al., 2020).
than the medical one. In urology practice, one hospital proposed an • In urological practice, a scheme of therapeutic options was proposed
algorithm to classify procedures for oncological diseases into non-de- by a group of experts (Fizazi and pour les membres du bureau du
ferrable (such as muscle invasive bladder cancer, high risk locally ad- Groupe d’étude des tumeurs uro-génitales, 2020) that meet the
vanced prostate cancer); deferrable (such as partial nephrectomy for proposed guidelines of the CCAFU (Comité de Cancérologie de
cT1a renal cell carcinoma), semi-non-deferrable (elective procedures in l’Association Française d’Urologie (Mejean et al., 2020): maintain
a low disease burden hospital) and replaceable by other treatments, treatment of every curable disease with possible delay of surgery for
while taking into consideration patients comorbidity profiles and hos- very small stable renal tumors, encourage active surveillance for low
pitals resources (Ficarra et al., 2020). Telephone screening of patients risk prostate cancer, privilege neoadjuvant hormone therapy with
for any suspicious symptom before admission for elective procedures is differed radiotherapy for intermediate or high risk localized prostate
also recommended by a group of practitioners, with a low threshold for cancer over surgery, discuss neoadjuvant chemotherapy for oper-
undergoing nasopharyngeal swabs before surgery (Simonato et al., able bladder cancer and choose less toxic chemotherapy with use of
2020). In gastroenterology, a change in practice was also witnessed G-CSF to avoid neutropenia. As for advanced disease, those re-
(Pellino and Spinelli, 2020). For instance, in colorectal surgery, most commendations agree on minimizing the risk of immunosuppression
elective procedures were limited in many centers over the country, but by avoiding corticosteroids for prostate cancer, substituting highly
colorectal cancer surgeries were not part of this strategy and were myelotoxic protocols with fewer toxic ones (gemzar-cisplatin in-
maintained along with emergent procedures (Lisi et al., 2020; Di stead of MVAC) with G-CSF use. However, the safety of im-
Saverio et al., 2020). Some practitioners in rectal cancer opted, in the munotherapy for renal and urothelial carcinomas remains con-
absence of recommendations to substitute oral capecitabine for 5-FU troversial and should be discussed on a case-by-case basis.
whenever possible, and to adopt short course radiotherapy in the • In sarcoma, The French Sarcoma group issued recommendations
neoadjuvant setting with delaying surgical interventions (De Felice and that encourage maintaining neoadjuvant and adjuvant che-
Petrucciani, 2020). motherapy and radiotherapy for all patients who are not suspected
An algorithm was also proposed by a northern Italian group of ra- to have a SARS-CoV-2 infection, and advise to ensure post-operative
diation oncology that insisted on continuing to deliver treatment for resuscitation capacities for high risk surgeries (Penel et al., 2020).
cancer patients with adoption of hypo fractionated protocols whenever
possible, while withholding radiotherapy for benign disease or post- 3.4.4. International guidelines and recommendations
poning it if possible, in the adjuvant setting, and withholding treatment Recently, a huge effort was made by various oncology societies and
only for confirmed or highly suspicious cases of COVID-19 (Filippi national authorities to implement recommendations that help practi-
et al., 2020). tioners in decision making on cancer care during the SARS-CoV-2
After reviewing the above resources, we conclude that efforts are pandemic. An international collaborative group reviewed the chal-
gathered to establish management strategies in Italy, but no tool is lenges encountered in cancer care and proposed some practical mea-
available to date to test the efficacy and safety of these propositions. We sures for the management of cancer patients based on the available data
encourage creating tools to validate these protocols in the future. on the 26th of March (Al-Shamsi et al., 2020). International guidelines

6
E. Moujaess, et al. Critical Reviews in Oncology / Hematology 150 (2020) 102972

were issued with common general principles, and few particularities COVID-19 infection.
that emerge from every society’s experience (Burki, 2020b).
4. Conclusion
• In hematology, researchers are most interested in hematopoietic
stem cell transplantation, first because of a higher risk of infection in In spite of all the efforts that are made, finding the ideal approach
neutropenic patients, and second because of the risk carried by stem for cancer patients in the middle of the threat of the COVID-19 is not
cells donation, transportation and preservation as well as the diffi- evident. As we are writing this paper the number of cancer patients
culty to find donors with travel bans (Szer et al., 2020; Dholaria and tested positive is increasing, the capacity of some cancer centers is
Savani, 2020). A reported case of a Chinese patient who was treated overwhelmed, and new guidelines are being issued by local and na-
with Cyclosporine A seven months following a bone marrow trans- tional authorities. The approach of cancer patients must be dynamic
plantation for AML and who died after acquiring a COVID-19 in- and tailored to every patient’s condition, every hospital’s resources and
fection despite getting adequate care suggests that physicians should every physician’s experience. Oncologists must keep in mind that be-
rethink the transplantation practice during the pandemic. The Eur- yond any scientific speculations, if the COVID-19 outbreak extends, the
opean Society of Blood and Marrow Transplantation EBMT issued risk of unavailability of high-level care in oncology would be greater
recommendations to protect patients during the COVID-19 out- than that of a SARS-CoV-2 infection in a cancer patient.
break. They consist of differing transplantation for confirmed cases
at least 3 months for low risk disease or until recovery for high risk Declaration of Competing Interest
disease. Symptomatic patients should be screened with multiplex
PCR (with or without COVID-19 RT-PCR) and the intervention The authors confirm that they do not have any conflict of interest.
should be differed if possible. Deferral also applies for patients who
have close contact with a positive case (and is strongly re- References
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