Since the COVID-19 pandemic showed up, the therapeutic and prognostic impact of COVID-19 infection on cancer patients has been evaluated (Curigliano et al., 2020; Liang et al., 2020; Sociedad Española de Oncología Médica [SEOM], 2020; Trilla, 2020; World Health Organization [WHO], 2020), suggesting a higher mortality and higher risk of developing complications (Saini et al., 2020). The greater physical vulnerability of cancer patients infected with Sars-Cov-2 seems to be related to the state of immunosuppression associated, caused by the tumor process itself and by the administration of antineoplastic treatments, the presence of comorbidities, and the need to regularly visit a hospital (Miyashita et al., 2020; Petrova et al., 2020; Zhang et al., 2020). At Hospital Universitario de La Princesa we recently published a mortality rate for COVID-19 disease in cancer patients of 33% (Toquero Diez et al., 2020), similar to that reported in other national and international centers (Lee et al., 2020).

Most studies in cancer patients infected with COVID-19 have focused on the clinical course and treatment of the infection (Wang and Zhang, 2020; Zhang et al., 2020). However, we do not have studies addressing the emotional impact that the first wave of the pandemic has had on oncology patients who were under active treatment, and who, therefore, regularly attended a hospital center during Spain’s strictest months of lockdown and worst epidemiological situation of the pandemic.

Psychopathological disorders (emotional distress, anxiety, and depression) in cancer patients are frequent and exceed those observed in the general population (Pitman et al., 2018). Moreover, they differ widely according to the stage of the oncological disease, type of patient (ambulatory or hospitalized), treatment received, and various social, psychological, and physical factors (Hernández et al., 2013). Several studies have been carried out in the oncologic population evaluating psychopathological symptomatology (Moncayo et al., 2008; Hernández and Antonio Cruzado, 2013; Hernández et al., 2013). Despite differences in the development and interpretation of the results, all have shown the importance of the psychological approach in the comprehensive treatment of cancer patients, especially in the most vulnerable. This has also been demonstrated in the context of other epidemics. Studies evaluating the emotional impact of the SARS epidemic in 2004 or Ebola in 2014 have shown a worsening in psychological symptomatology rates in the global population, and to a greater extent, among the most vulnerable groups such as cancer patients (Brooks et al., 2020). Therefore, the COVID-19 pandemic is likely to magnify mental health problems in cancer patients (Agua et al., 2020; Swainston et al., 2020; Wang et al., 2020).

The studies published to date about the emotional impact caused by the COVID-19 pandemic in oncology patients are scarce, and the different studies have important methodological differences, mainly due to the use of different scales for measuring psychopathological symptomatology (HADS, CES-D, GSDS, etc.)—some of which are not clearly validated in this type of population—and also because they used different cut-off points. The studied populations are heterogeneous (patients with cancer under active treatment or follow-up, long survivors, different types of tumors or tumor stage, etc.), which make it difficult to compare or extrapolate conclusions (Agua et al., 2020; Letaief-Ksontini et al., 2020; Miaskowski et al., 2020; Swainston et al., 2020; Wang et al., 2020). In this regard, rates of depression and anxiety in cancer patients reported during the COVID-19 pandemic vary widely between 11.8–35.3 and 9.9–69.2%, respectively (Agua et al., 2020; Letaief-Ksontini et al., 2020; Lou et al., 2020; van de Poll-Franse et al., 2020; Wang et al., 2020; Gultekin et al., 2021; Mogami et al., 2021).

In our knowledge, this is the first prospective study to evaluate the emotional and social implications of the COVID-19 pandemic in cancer outpatients who were on active treatment exclusively, and who regularly attended a hospital center during the first and arguably most impactful wave of the COVID-19 pandemic. Thus, the main objective of this study is to explore the level of emotional distress and anxious and/or depressive symptomatology of oncology patients during the first wave of the COVID-19 pandemic, and subsequently, to study the relationship between psychological symptomatology of these patients and a range of sociodemographic, clinical, economic, and spiritual factors.

This project is the first study that addresses the emotional impact that the COVID-19 pandemic had on cancer patients who were under active treatment in the oncohematologic DH of the Hospital Universitario de La Princesa, during the first and harder stage of the COVID-19 pandemic (March-June 2020) in Madrid.

We detected an emotional distress rate of 52.8%, anxiety of 42.3%, and depression of 58.6%. Previous evidence on psychopathological symptomatology in outpatients with cancer is scarce. Furthermore, the presence of important methodological differences between studies makes the results difficult to compare (Carroll et al., 1993; Grassi et al., 2004; Annunziata et al., 2020). However, Moncayo et al. (2008) described the prevalence of emotional distress, anxiety and depression in the oncology population under active treatment using a methodology similar to ours, and therefore we use it as historical control to obtain an adequate comparator due to the impossibility to guarantee a correct randomization of patients during the first wave of the pandemic. The Gil-Moncayo study analyzed 400 ambulatory cancer patients, using the HADS scale as a screening method, and used the same cut-off points as in our study. They described a rate of emotional distress of 42.5% (HADS-T), anxiety of 36.5% (HADS-A), and depression of 45% (HADS-D) (Moncayo et al., 2008). Comparing these results with those at our center, we detect a clinical and relevant increase in the levels of emotional distress, anxiety, and depression in the outpatient oncology population in accordance with the non-pandemic situation and previously published literature (Moncayo et al., 2008), but these results were not statistically significant (Z score; p = 0.06). Despite a greater tendency, we consider that the increase detected was moderate, considering the profound psychological impact that COVID-19 pandemic has had on society worldwide, causing a significant increase in the rates of emotional distress, anxiety, and depression in the general population according to various studies (Pierce et al., 2020; Xiong et al., 2020).

Apart from our study, little evidence has analyzed the real impact from this pandemic on cancer patients and it may take several years to understand the real psychopathological implications in this population. Furthermore, there are important methodological discrepancies (different type of target patients, different scales for measuring psychopathological symptomatology, different endpoints, etc.) with heterogeneous results that are difficult to compare (Agua et al., 2020; Letaief-Ksontini et al., 2020; Lou et al., 2020; Swainston et al., 2020; Wang et al., 2020) (Table 5). Most of these studies carried out on cancer patients have detected an increase in perceived levels of anxiety, depression, and global discomfort, highlighting the importance of the emotional sphere in their comprehensive treatment (Agua et al., 2020; Letaief-Ksontini et al., 2020; Lou et al., 2020; Swainston et al., 2020; van de Poll-Franse et al., 2020; Wang et al., 2020; Gultekin et al., 2021; Mogami et al., 2021). In our study it is striking how the greatest concern of oncology patients continues to be their tumor—even more than the COVID-19 pandemic itself. Of 104 patients included in the study, 51% expressed greater fear of their tumor compared with coronavirus infection, which seems to indicate that the condition of being an oncology patient, exposed to end of life considerations, has a greater impact than contracting COVID-19 or the consequences of this disease. These data coincide with that published by Gultekin et al. (2021) in their study, where 58% of patients expressed greater fear of their tumor vs. COVID-19.

The observed rates of emotional distress, anxiety, and depression, which are close to pre-pandemic levels, may be related to several factors: (a) the time at which the study was conducted—late May and early June 2020, when the pandemic had already entered a de-escalation phase and care pressure had decreased significantly in Madrid so that the perception of fear had been reduced in the population; (b) the need for patients to visit a hospital center regularly to receive treatment, allowing them to have closer contact with health personnel (doctors, nurses, and team of psychologist of AECC), and to resolve their questions and concerns about the COVID-19 pandemic with medical staff directly. Studies in non-oncologic populations without regular contact with hospital staff have shown higher levels of psychopathological symptomatology (Parrado-González and León-Jariego, 2020; Talevi et al., 2020).

The factors significantly related to higher rates of emotional distress, anxiety, and depression were previous consumption of psychotropic drugs and the adoption of greater prevention measures than those recommended for general population to avoid the infection because they considered at higher risk of developing more severe complications by the COVID-19. A worsening of patient’s financial situation during the pandemic was associated with greater distress and depression, the use of alternative therapies and Religion with greater anxiety and depression, lower educational level with greater depression, and frequent exposure to the media with a higher level of anxiety. This data is consistent with that published in other studies, such as that of the Spanish Association Against Cancer (AECC) (Agua et al., 2020) or Wang et al. (2020), where a worsening financial situation, frequent exposure to the media, and greater concern about COVID-19 infection were shown to be risk factors associated with higher rates of psychopathological symptomatology. This seems to demonstrate that, although the media is useful to increase the level of information in society, at other times it can transmit contradictory or excessive information (Bendau et al., 2020; Joshua Morganstein, 2020). These results are also consistent with those published by the AECC study, where up to 50% of patients who were unable to disconnect from the media presented high levels of emotional disturbance (Agua et al., 2020).

Although not significantly, younger patients (those under the age of 65) presented higher levels of psychological symptomatology, something which could be explained by the fact that younger patients are more shocked by the COVID-19 disease than older, according to what has been previously published (Linden et al., 2012; Kim et al., 2013). Similarly, being female, single, having a previous diagnosis of psychiatric illness, lack of information about COVID-19, and lack of social or family support during the pandemic were also factors related to higher rates of emotional distress, anxiety, and depression, although not significantly—results similar to those published by Wang et al. (2020) and Gultekin et al. (2021).

No significant differences were found in the rates of psychopathological symptomatology according to tumor type, oncologic stage, or treatment administered in either the subscales (anxiety or depression) or in the global emotional distress scale, suggesting that the emotional impact of the COVID-19 pandemic was similar for all cancer patients, regardless of the stage of their disease. This finding is similar to the results published by Gultekin et al. (2021). The rescheduling of treatments or the delay of any of the treatment cycles did not have a negative impact on the emotional sphere, data which agrees with that published by Letaief-Ksontini et al. (2020). However, other studies have shown varying results, as in the study by Swainston et al. (2020), carried out on a English population of women with breast cancer (any stage and any type of treatment), which showed that those women who experienced disruptions to their oncology services had higher levels of general anxiety, depression, and COVID-19 related emotional vulnerability (Swainston et al., 2020).

Among the limitations of this study, we should take into consideration some weak points which could be considered in future lines of research. In terms of methodology, the main limitations are the unicenter design and the lack of randomization to obtain an adequate control group to compare our results. Because the Pandemic was a worldwide event experienced by the entire population at the same time, it was not possible to ensure the randomization of patients. The evaluation method used also presents some considerations that are important to point out. Although the questionnaire applied (HADS) is a simple and intuitive tool that has shown adequate psychometric properties to evaluate anxiety, depression and emotional distress symptomatology in the general population (Herrero et al., 2003), also in oncologic patients (Snaith, 2003; Grassi et al., 2004; Moncayo et al., 2008; Mitchell et al., 2010; Chapman et al., 2020; Swainston et al., 2020) it is only self-report questionnaire and did not evaluate other psychological and personality aspects that might play a role in psychological distress of cancer patients. It would therefore be advisable to include other measures related to this distinction in future research on cancer patients, giving special importance to face-to-face interviews with the patient as well as other negative consequences of the pandemic on oncology patients, such as the job insecurity created by the COVID-19 outbreak in oncology patients by not being able to attend their usual work because of their increased vulnerability, which could increase the risk of experiencing affective disorders (anxiety and depression) and worse cognitive function in cancer patients (Chapman et al., 2020). Finally, levels of emotional distress, anxiety, and depression may have varied throughout the pandemic, whereas our study was conducted only during the first wave, it might be interesting to replicate this study in the current pandemic situation.

The results of this study show the importance of increasing the accessibility of mental health services to cancer patients. It is urgent to focus the efforts and economic resources of future governments on guaranteeing adequate care for the psychological consequences of the COVID-19 pandemic, especially in the most vulnerable population, such as oncology patients (Chapman et al., 2020). Future research should continue to monitor the long-term effects of COVID-19 on the psychological health of cancer patients (Swainston et al., 2020).

The COVID-19 pandemic has been a game changer in healthcare worldwide. Oncology patients are an at-risk population that needs special attention and care, and further studies are needed to help us improve and optimize the treatment of this infection in oncology patients. In our study, high rates of emotional distress have been detected during the first wave of the COVID-19 pandemic among cancer patients in active treatment, this was higher and clinically relevant than observed in a comparable population (42.5%), although not significant. Although cancer continues to be the main fear of oncology patients, it is also essential to know the impact of COVID-19 pandemic on the emotional sphere in order to ensure a holistic approach for these patients, and to increase efforts to make mental health services more accessible to cancer patients.

The datasets presented in this article are not readily available because due to privacy or ethical restrictions. Requests to access the datasets should be directed to PT, kiku.toquero@gmail.com.

The studies involving human participants were reviewed and approved by Drug Research Ethical Committee (CEIm) of the Hospital Universitario de La Princesa (registration number “4122,” approved 22-05-20, CEIm 12/20). The patients/participants provided their written informed consent to participate in this study.

PT, CB, ML, BH, RC, and NR-L: conception and design. PT, CB, ML, BH, EBV, AGG, EM, OD, AB, JS-T, PC, RM, RC, and NR-L: provision of study material or patients. PT, ML, BH, EBV, AGG, EM, OD, AB, JS-T, PC, RM, RC, and NR-L: collection and/or assembly of data. PT, CB, ML, RC, and NR-L: data analysis and interpretation and manuscript writing. PT, CB, ML, BH, EBV, AGG, EM, OD, AB, JS-T, PC, RM, RC, and NR-L: final approval of manuscript. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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