key: cord-0723270-1kmt0t86
authors: Moujaess, Elissar; Kourie, Hampig Raphael; Ghosn, Marwan
title: Cancer patients and research during COVID-19 pandemic: A systematic review of current evidence
date: 2020-04-22
journal: Crit Rev Oncol Hematol
DOI: 10.1016/j.critrevonc.2020.102972
sha: ad5abad2c6fb3775437f7aa725cd78995f5f3bba
doc_id: 723270
cord_uid: 1kmt0t86

Abstract The novel coronavirus, also known as SARS-Cov-2 or COVID-19 has become a worldwide threat and the major healthcare concern of the year 2020. Cancer research was directly affected by the emerging of this disease. According to some Chinese studies, cancer patients are more vulnerable to COVID-19 complications. This observation led many oncologists to change their daily practice in cancer care, without solid evidence and recommendations. Moreover, the COVID-19 manifestations as well as its diagnosis are particular in this special 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.

The novel coronavirus, also known as SARS-Cov-2 or COVID-19 has become a worldwide threat and healthcare concern. Human to human transmission of the virus occurs through respiratory droplets (by coughing or sneezing) and through direct contact with an infected patient or indirect contact with fomites in his environment (1, 2) . Since its outbreak in China at the end of 2019 and until the 5 th of April 2020, the pandemic has affected more than a million of people and caused 62773 deaths globally (3). It is thought that patients with comorbid conditions are more susceptible to manifest complications of the viral infection (4) . According to a recently published Chinese cohort, patients with cancer had a higher risk of developing severe events (intensive care unit admission, invasive ventilation, or death) compared with patients without cancer (39% vs 8%, p=0·0003) (5) . Moreover, public health measures that are implemented in order to control the disease spread aim to decrease preventable hospital admissions and elective procedures (6) .

However, cancer patients need continuous care, and undergoing diagnostic tests or therapeutic interventions is not a luxury, whereas their potential COVID-19 exposure could be very risky, or even fatal. Remarkable efforts are made to understand the particularity of cancer patients who contract the novel coronavirus, to overcome the diagnostic and therapeutic challenges and to implement recommendations to protect this vulnerable population from the virus exposure as well as from the disease progression resulting from testing and treatment delays. In this article, epidemiological, radiological and clinical features of adult cancer patients with COVID-19 will be reviewed based on an extensive review of the literature, as well as diagnostic and therapeutic strategies suggested by healthcare providers and institutions in endemics areas, particularly China and Italy.

In order to review the particularities of COVID-19 in adult patients with cancer, an extensive electronic search of the literature was conducted in the PubMed database until the 5th of April 2020. The following keywords with Boolean operators were used 'covid-19', 'novel coronavirus'

and 'SARS-CoV-2' in combination with 'cancer', 'neoplasm', 'oncology' and 'malignancy'. A total of 223 articles were extracted. We included articles in English as well as articles in French because we are familiar with this language. Abstracts in English of articles in Chinese language were also J o u r n a l P r e -p r o o f 3 included. Duplicated articles and articles that were published before the era of SARS-Cov-2 (i.e., before December 2019) were excluded. Titles and abstracts of retrieved articles were screened for eligibility, and then entire texts were analyzed and 88 papers that respond to our objectives were included in this review. Our work is summarized in the PRISMA diagram below.

Out of 88 articles, six were in French language and 19 were in Chinese language with English abstracts. Most of the papers consisted of short editorials, letters, correspondence or comments.

Ten Cohort studies were identified (retrospective, prospective or cross-sectional analysis) 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 from China and Italy.

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 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 Researchers in oncology are preoccupied by more than one aspect of the COVID-19. Subjects of interest in the papers that were included in this review could be divided in four categories :

 Cancer research in the era of COVID-19, and the effect of cancer therapy on COVID-19 patients (6 articles). thalidomide, the PD-1 inhibitor camrelizumab and other anti-cancer agents in the treatment of SARS-CoV-2 infections. The potential benefit of other targeted therapies such as afatinib, carfilzomib and ixazomib was highlighted in the literature (9) .

Many other cancer drugs are being investigated in this field. For example, a theoretical role of kinase inhibitors in the reduction of infectivity of well-known viruses such as Ebola and Hepatitis C is described, suggesting that drugs like sunitinib and erlotinib would potentially be effective against SARS-CoV-2 (10).

Moreover, a group of researchers used network proximity analyses of drug targets and virushost interactions in the human interactome to identify repurposable drugs and potential drug combinations for the treatment of SARS-CoV-2. Three combinations were deemed effective: sirolimus plus dactinomycin, mercaptopurine plus melatonin, and toremifene plus emodin, all of which consisting of at least one anti-cancer agent (an immunosuppressant, an antineoplastic agent and a selective estrogen receptor modulator respectively) (11) .

Amidst this rapid evolution of the COVID-19 should be kept in mind the need to respect some clinical research ethics. In fact, the medical ethics editorial team of The Oncologist focused on three crucial considerations in cancer research. First one is non-abandonment of a patient whose prognosis and wellbeing is dependent on an investigational treatment and a protocol to which he is adhering. Second one is making an effort to flatten the curve of COVID-19 infection by minimizing any unnecessary exposure to a suspicious environment. Finally they emphasize on psychosocial support of the patient and of the research team in the middle of the outbreak (12) .

At the beginning of the epidemic in China, multiple epidemiological studies were conducted to 3 of these 10 patients had a severe presentation on admission while the others had mild symptoms (13) . Another Chinese retrospective cohort studied 69 cases of COVID-19 in Wuhan.

Disease severity at presentation was assessed by the SpO2 as the sole criteria, with a cutoff of 90%. Among these 69 patients, four had a history of malignancy of whom only one patient presented with an SpO2 <90% (14) .

In both cohorts previously cited the number of patients who had a severe presentation was higher than that of less severe cases, but this observation did not apply to the sub-group of patients with malignancy. However, these data are not enough to conclude that cancer patients tend to present with milder symptoms than the rest of the population.

Liang et al were the first to publish data regarding cancer patients who are diagnosed with COVID-19. Their Chinese cohort was the largest and the only prospective cohort to date interested in oncology patients. It included 1590 COVID-19 cases of whom 18 (1%; 95% CI 0·61-1·65) had a history of cancer. This was higher than the incidence of cancer in the overall Chinese population (0·29%). The most frequent primary tumor was lung cancer. Four of 16 patients had received chemotherapy or surgery within the prior month, and twelve were in remission at the time of the infection. The mean age was 63·1 years in cancer patients vs 48·7 years in non-cancer patients. There was no difference in gender between the two groups. Clinical presentation was marked by more polypnea in the cancer group (47% vs 23%), and imaging findings by more severe CT scan at baseline (94% vs 71%), without significant difference in severity on chest X-ray (5) .

These data were helpful in clarifying epidemiologic and clinical features of cancer patients during the COVID-19 pandemic, but were criticized by Wang et al: the higher incidence of cancer in this cohort compared to that of cancer in the general Chinese population was interpreted as an increased risk for cancer patients to be infected with the COVID-19. However, only four of the 18 patients had a disease that is actively treated while twelve were in complete remission and two had an unknown treatment status. Therefore their infection might be related to another etiology than their cancer (15) . infection with diffuse, irregular, small ground-glass opacities with partial consolidation on day 10 of infection on chest CT-scan. This is not compatible with the typical peripheral subpleural ground-glass infiltrates (18) .

 Cancer patients might have radiographic findings similar to those of a SAR-CoV-2 infection and can be misleading. A Chinese article reported the cases of five of 139 cancer patients who had ground-glass opacities on baseline chest CT-scans. Three of these patients underwent RT-PCR, had a negative test and were considered negative for COVID-19. The most retained diagnosis in these patients was another viral infection (19) . Nevertheless, many sources now admit that radiographic findings are more sensitive than RT-PCR in J o u r n a l P r e -p r o o f detecting COVID-19 (20) and the previously reported cases could have a COVID-19

infection that was missed because of a false negative PCR test.

 Due to the high frequency of routine chest imaging in the follow up of cancer patients, incidental findings suggestive of COVID-19 may not be infrequent. These findings are a source of frustration for the patient and the physician, as they may suggest either another differential diagnosis or a COVID-19 infection at an early asymptomatic stage especially in regions of high disease prevalence as was the case of an Italian patient who was referred for an FDG-PET/CT (21) . This was then highlighted by an Italian analysis performed in a nuclear medicine center where incidental findings were recorded in 7 of 65 asymptomatic patients who underwent imaging studies, of whom 5 had a laboratory confirmed infection (22) .

 Due to similarity in symptoms between the infection and the underlying disease, especially in lung cancer patients and patients with pulmonary metastasis, the diagnosis of COVID-19 may be delayed. In two patients who were programmed for elective lobectomy for early stage lung cancer in China, a retrospective diagnosis of SARS-CoV-2 was made after patients worsened their symptoms post-operatively. The examination of pulmonary pathology showed that inflammatory changes consistent with interstitial disease were present at the time of surgery (23).

 Some clinical and biological features can mask a COVID-19 presentation in cancer patients. This is the case of hematologic malignancies where laboratory results can be misleading. For instance, a Chinese patient with a history of non-Hodgkin lymphoma and CLL treated with chlorambucil presented with signs of disease progression as well as respiratory symptoms. She initially denied any exposure to a confirmed case, and the diagnosis of COVID-19 was delayed because of the high white blood counts count (91·85 × 109 cells/L) and the focus on the treatment of his underlying malignancy (24) .

Few studies that analyze the impact of a SARS-CoV-2 infection on patients with malignancy were found in our literature review. However, we can make some conclusions from cohort studies that included cancer patients.

A study performed on 24 critically ill patients in Seattle found that most of these patients had comorbid conditions, however a history of cancer was not found in any of these patients (25) .

We know that this is a very small sample, but we still can tell that patients who have other underlying chronic conditions such as asthma or diabetes might be more concerned about becoming critically ill if infected with the SARS-CoV-2 than cancer patients.

An analysis of the first 1975 COVID-19 patients in China was performed, and the first 17 deaths were reviewed. Most of the cases who 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 patient had a history of cancer. He was an 86-year-old man with a history of colon cancer and underwent a colon cancer surgery (26) . Of course, this small sample prevents us from extrapolating these data; however, this patient had other comorbid conditions (hypertension and diabetes mellitus) that, along with his age and male gender make him more vulnerable to a SARS-CoV-2 infection.

In fact, a nationwide analysis of 1590 COVID-19 hospitalized patients in 575 Chinese hospitals between December 11th, 2019 and January 31st, 2020 showed that the most prevalent comorbidities were hypertension (16.9%) and diabetes (8.2%). Only 18 patients (1.1%) had a history on malignancy. However, severe cases in this analysis were more likely to have a malignancy (50.0% versus 15.6%) compared with non-severe cases. The composite endpoints consisting of admission to intensive care unit, or invasive ventilation, or death were also analyzed, and after adjustment for age and smoking status a history of malignancy was the fourth most common risk factor of reaching the composite endpoints with a HR of 3.50 (95%CI 1.60- 

We believe that these results should be interpreted with caution in the absence of adjustment to the prevalence of the different comorbidities in the Chinese population.

The nationwide cohort of Liang et al previously described, specifically targeting cancer patients, concluded that this population was predisposed to higher risk of severe events (ICU admission, mechanical ventilation or death) compared to non-cancer patients (39 vs 8%; p = 0.0003), and that among cancer patients, those with a recent history of chemotherapy or surgery had a higher risk of severe events than those who did not receive treatment (5) . These data should also be carefully interpreted, not only because of the small sample, but also because cancer patients in this cohort had a significantly older median age than their control (63·1 vs 48·7 years) as well as a more significant history of smoking, suggesting that these two factors might be more associated with worse COVID-19 outcomes than the cancer history itself (15) . This said, some authors suggest that because no solid evidence exists yet, treatment modification or interruption should not be a standard and should be individualized and discussed with every patient (31).

While every cancer patient and his healthcare provider are concerned about the risk of transmission of COVID-19 in hospital settings, the risk of disease progression with treatment delay started to become more serious with the pandemic persisting (32) (33) (34) (35) , and the healthcare system distraction towards COVID-19 might have harmful consequences on cancer patients (36) .

The urgent need for guidelines implementation to protect cancer patients from acquiring a COVID-19 without harming them is discussed by many authors in the literature. In the absence of universal guidelines, most of the strategies adopted involve prioritizing urgent situations such as acute leukemia, curative treatments for aggressive diseases, and adjuvant and neoadjuvant therapies while withholding or postponing palliative therapies for poor prognosis patients (37) .

Telemedicine is also encouraged (38) . Measures to protect medical staff are proposed because this indirectly impacts patients' safety. These measures consist of prioritizing laparoscopic procedures in cancer surgery to minimize the exposure to aerosolized specimen (39) and limiting endoscopic diagnostic procedures to the necessary with application of strict protective measures J o u r n a l P r e -p r o o f particularly in bronchoscopy (40) . Some medical and imaging oncology wards were completely re-organized to safely accommodate cancer patients (41-43).

Since the outbreak of SARS-CoV-2 in China, the whole healthcare system was shifted towards the management of SARS-CoV-2 patients. Chinese oncologist faced difficulties in providing the best care for their patients. We add to this that integrative cancer therapy that involves close contact of the care provider with patients is widely available in China and constitutes a great risk during the pandemic (44) . As of the 1 st of February, almost a month following the declaration of the epidemic, more than a dozen of articles that propose management strategies for oncology patients were published. Most of these articles have their bodies in Chinese. Abstracts of these articles were reviewed to form a picture of the oncology practice in China during the COVID-19

pandemic. Common to all works was the encouragement of a multidisciplinary approach and the delay of every elective procedure. However, the definition of elective procedures is not universal (45) .

Most of the Chinese literature emphasized on gastrointestinal tumors, especially the surgical management (46) (47) (48) (49) . A COVID-19 positive patient with early stage colon cancer was successfully treated with colectomy without complications after receiving anti-viral therapy and negating his RT-PCR on two occasions (50) . Since fecal-oral transmission cannot be excluded to date, experts encourage laparoscopic techniques (46) , prioritizing non-surgical and interventional management such as stent placement for gastro-intestinal obstruction, avoiding endoscopic procedures (51) (52) (53) , providing isolation areas for invasive interventions for suspected or confirmed cases (51, 53) . As for the medical management, a group of experts suggested maintaining chemotherapy for metastatic patients, providing necessary treatment for patients who have a progressive disease and decreasing intensity and frequency of adjuvant chemotherapy (54) . Chinese physicians adopted modifications not only in the therapeutic strategies but also in the diagnostic procedures of cancer patients (55, 56) . Delaying gastrointestinal diagnostic procedures for patients with a stable disease was recommended by a group of practitioners (53) . Furthermore, outpatient care for breast cancer patients was also highlighted in one article (62) .

Another small Chinese study identified the lack of strict guides for the management of gynecological cancer in an endemic region (63) .

This said, China obviously witness a change in practice in the management of oncology patients during the COVID-19 pandemic.

After China, Italy was one of the first countries that experienced a tragic increase in the incidence and mortality rate of COVID-19 cases, with more than 100000 cases and up to 11600 deaths by Similarly, remote monitoring and home care were encouraged (66) . A group of practitioners in Tuscany, Italy, adopted and validated a home care protocol that consisted of a double triage to protect patients with cancer. The first triage aims to screen patients and their cohabiters for any J o u r n a l P r e -p r o o f 14 sign or symptom of a COVID-19 infection via a telephone interview, while a second telephone interview aims to schedule home access with variable frequency of visits based on symptoms burden and patient's prognosis (67) .

One article in the Italian literature highlighted the lack of recommendations that guide the diagnosis, follow-up and treatment of patients with head and neck cancer in the era of SARS-CoV-2 (68). As for lung cancer, practical suggestions appeared on the 27 th of March in the ESMO Open to guide physicians in making decisions on which treatment and procedure to prioritize (69) .

Most of the other Italian published works targeted urological and gastrointestinal tumors, also with more focus on the surgical aspect than the medical one. In urology practice, one hospital proposed an algorithm to classify procedures for oncological diseases into non-deferrable (such as muscle invasive bladder cancer, high risk locally advanced prostate cancer); deferrable (such as partial nephrectomy for cT1a renal cell carcinoma), semi-non-deferrable (elective procedures in a low disease burden hospital) and replaceable by other treatments, while taking into consideration patients comorbidity profiles and hospitals resources (70) . Telephone screening of patients for any suspicious symptom before admission for elective procedures is also recommended by a group of practitioners, with a low threshold for undergoing nasopharyngeal swabs before surgery (71) . In gastroenterology, a change in practice was also witnessed (72) . For instance, in colorectal surgery, most elective procedures were limited in many centers over the country, but colorectal cancer surgeries were not part of this strategy and were maintained along with emergent procedures (73, 74) . Some practitioners in rectal cancer opted, in the absence of recommendations to substitute oral capecitabine for 5-FU whenever possible, and to adopt short course radiotherapy in the neoadjuvant setting with delaying surgical interventions (75) .

An algorithm was also proposed by a northern Italian group of radiation oncology that insisted on continuing to deliver treatment for cancer patients with adoption of hypo fractionated protocols whenever possible, while withholding radiotherapy for benign disease or postponing it if possible, in the adjuvant setting, and withholding treatment only for confirmed or highly suspicious cases of COVID-19 (76) .

After reviewing the above resources, we conclude that efforts are gathered to establish management strategies in Italy, but no tool is available to date to test the efficacy and safety of these propositions. We encourage creating tools to validate these protocols in the future.

Practice of oncology in France was not different than that in China and Italy, but some French  In gynecological cancer, the FRANCOGYN group for the CNGOF propose recommendations that do not differ much from the standard of care, except that they emphasize on radio-chemotherapy in the first line setting for cervical cancer instead of surgical treatment, and on the neoadjuvant chemotherapy for advanced ovarian cancer even for tumors that are judged to be resectable in order to reduce high risk surgeries and long ICU stays (80) . Note that similar suggestions were proposed by a multinational group of practitioners (81) . 

Recently, a huge effort was made by various oncology societies and national authorities to implement recommendations that help practitioners in decision making on cancer care during the SARS-CoV-2 pandemic. An international collaborative group reviewed the challenges encountered in cancer care and proposed some practical measures for the management of cancer patients based on the available data on the 26 th of March (85) .

International guidelines were issued with common general principles, and few particularities that emerge from every society's experience (86) . o Providing emotional and physical support for healthcare workers, as well as protective measures for those of them who have chronic conditions that predispose them to the complications of the COVID-19 infection.

In spite of all the efforts that are made, finding the ideal approach for cancer patients in the middle of the threat of the COVID-19 is not evident. As we are writing this paper the number of cancer patients tested positive is increasing, the capacity of some cancer centers is overwhelmed, and new guidelines are being issued by local and national authorities. The approach of cancer patients must be dynamic and tailored to every patient's condition, every J o u r n a l P r e -p r o o f hospital's resources and every physician's experience. Oncologists must keep in mind that beyond any scientific speculations, if the COVID-19 outbreak extends, the risk of unavailability of high-level care in oncology would be greater than that of a SARS-CoV-2 infection in a cancer patient. 

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The authors confirm that they do not have any conflict of interest.