Abstract
Background: The COVID-19 pandemic has transformed breast cancer care for patients and healthcare providers. Circumstances varied greatly by region and hospital, depending on COVID-19 prevalence, case mix, hospital type, and available resources. These challenges have disrupted screening programs and have been particularly distressing for both women with a breast cancer diagnosis and their providers. Summary: This review explores the retrospective impact of the COVID-19 pandemic on primary breast cancer care. It analyzes changes in screening participation, diagnosis rates, treatment modalities, and the delivery of psycho-oncological support during the pandemic. The study found a significant reduction in breast cancer screenings and a subsequent stage shift in diagnoses, with fewer early-stage and more advanced-stage cancers being detected. Additionally, the review discusses the psychosocial challenges faced by patients and the adaptations made in care delivery, such as the increased use of telemedicine. Despite these challenges, the healthcare systems showed resilience, with core treatment services largely maintained and rapid adaptations to new care models. Key Messages: There was a marked decrease in breast cancer screenings and early diagnoses during the pandemic, with a shift toward more advanced-stage detections. While there was an increased use of neoadjuvant therapies and telemedicine, essential breast cancer treatments were mostly sustained, reflecting the resilience of healthcare systems. The pandemic significantly impacted the mental health of breast cancer patients, exacerbating anxiety and depression and highlighting the need for improved psycho-oncological support. The full impact of these disruptions on long-term breast cancer outcomes remains uncertain, necessitating ongoing monitoring and adaptation of care strategies to mitigate adverse effects.
Introduction
The outbreak of COVID-19 forced rapid decisions to face the needed healthcare response. A shutdown of healthcare services was necessary for COVID-19 management globally. Concerns about this impact as well as the redesign of clinical services, redistribution of resources, and changes in treatment priorities are still discussed. Breast cancer practice is based on different stages of care: screening programs, diagnostic assessments, surgery, adjuvant and neoadjuvant treatments, and radiotherapy [1, 2]. The interruption by the lockdown led to a reorganization of hospital departments: simplifying the diagnostic procedures, reducing non-urgent medical care, limiting or postponing in-person examinations, and introducing telephone or online assessments, resulting in higher flexibility in primary cancer care [3‒6]. All modifications to the gold standard have been made with unknown risk, based on expert opinion and existing evidence.
Following global recommendations, breast cancer screening, diagnosis, inpatient care, treatment, aftercare, and follow-up continued at limited capacity but were prioritized according to medical necessity. All treatment changes are particularly critical for cancer patients due to their increased susceptibility to infection and disease progression. A multitude of medical treatments result in immunosuppression, which consecutively elevates the risk of contracting COVID-19 and subsequently experiencing higher morbidity or mortality [3, 7, 8]. Given these factors and the need to minimize adverse events in cancer patients while maintaining treatment continuity, clinicians are faced with the challenge of balancing cancer care with infection control. Although the primary focus during the pandemic has been on managing and treating COVID-19 patients, it is crucial to comprehend the specific effects this pandemic had on breast cancer patients. In this literature review, we focus on the impact of COVID-19 on screening, diagnosis impact, guidelines, surgery, stage shift, psycho-oncology, and survivorship in primary breast cancer.
Methods
Search Strategy
The literature search was conducted in the PubMed databases using a predefined search algorithm. Different search algorithms were utilized for meta-analyses, randomized control trials, systematic reviews, reviews, observational studies, cohort or cross-sectional studies and studies by certified centers. We combined a search strategy of free-text terms and MeSH headings for the topic “breast cancer and COVID-19” combined with screening, diagnosis impact, guidelines, treatment, surgery, stage shift, aftercare, psycho-oncology, and survivorship. The search strategy included MeSH terms in combination with the basic search of “sars cov 2” OR “covid 19” AND “breast neoplasms,” followed by one of the specific topics: AND “psycho oncology”; AND “diagnosis” OR “mass screening” OR “early detection of cancer”; AND “aftercare”; AND “guidelines as topic”; AND “time”; AND “clinical trials as topic”; AND “neoplasm staging”; AND “therapeutics” OR “therapy”; AND “survivorship.” Additional relevant topics were identified through cross-referencing the citation lists of retrieved articles. The searches were performed up to June 9, 2023, exploring evidence published from January 1, 2020, onward (Fig. 1). No restriction on publication status was applied.
Eligibility Criteria
From the 1926 primary hits, relevant studies were selected based on the predefined inclusion and exclusion criteria, initially at the title and abstract level, followed by the full-text level (Fig. 1). The selection criteria for screening titles and abstracts were as follows: (1) availability of full-text primary reports (2) evidence-based meta-analyses, randomized control trials, systematic reviews, reviews, observational studies, cohort or cross-sectional studies, studies by certified centers; (3) reporting primary data on topics declared in the chapter above; (4) reports of German official registry sites (5) studies and reports published in English or German. Records of studies that did not include measures of outcomes of interest or quality were excluded, as well as those that did not consider the impact of COVID-19. Two authors (M.N. and M.P.) independently screened and evaluated the retrieved titles, abstracts, and full-texts for inclusion. Any discrepancies were resolved through discussion and consultation with a senior author (T.N.F. and B.B.). Additional experts were consulted for specific subject areas (F.D., N.K., S.M., E.R., and E.C.S.‐I.). Baseline characteristics were extracted for each included article, including the first and last author’s name, year and country of publication, study design, source of information, and study topic (online suppl. Table 1; for all online suppl. material, see https://doi.org/10.1159/000541015).
Results
Outpatient Care Sector
Screening in First Care
Due to the COVID-19 pandemic, many patients were not able to participate in early detection programs. Reduced office hours in outpatient medical practices, practice closures during the period of lockdown and contact restrictions changed the management of screening examinations and regular early detection programs. Particularly, elderly women (76.1% of pre-COVID-19), especially minorities, faced greater declines, and limited recovery in breast cancer, exacerbated by higher COVID-19 mortality and severe infection rates [9, 10]. Additionally, the fear of COVID infection led to a decline in clarification of symptoms and preventive measures. Compared with all other racial groups, Asian women experienced the largest decrease in screening mammography (72.5% of pre-COVID-19) and diagnostic mammography. These groups were already disadvantaged regarding healthcare access. The pandemic exacerbated these existing disparities, leading to further reductions in screening participation [10‒12].
This could have an impact on further treatment and diagnosis. Several studies have been published with heterogenous observations on the effect of the pandemic on breast cancer screening, its impact and need to be discussed. Mast et al. analyzed the pooled data from 60 US healthcare organizations for participation in cancer screening programs. During the pandemic peak between March 15 and June 16, 2020, 285,000 breast exams were missed, which represents a deficit of >63% relative to the number of screenings that would be expected based on the historical average. Focusing on the acute lockdown period, the high impact and decrease on mammography screening programs generally as well as in particular the German mammography screening program, could be determined [11, 13, 14]. The study types are summarized in Figure 2, and details for each included study are provided in online supplementary Table 1.
On average, 30% of female patients consistently and dependably engage in early detection programs in Germany [15]. However, amid the COVID-19 pandemic, planned asymptomatic consultations faced disruptions. An analysis encompassing all Germany-wide billed statutory health insurance services for mammography screening from 2019 to the first half of 2022 was conducted (refer to Fig. 3) [16]. The most pronounced impact was observed during the lockdown in April 2020, as depicted in Figure 2a and b. This resulted in a monthly missed appointment rate of −9% for the year 2020, as shown in Figure 2d, with a total of 250,437 fewer screenings compared to 2019 (Fig. 3c). Notably, a rebound effect began in May 2020, leading to a subsequent catch-up in missed screenings, as seen in Figure 2b. In comparison to 2019, there was a monthly increase of +5%, and a total of 107,245 additional screenings were documented for 2021 (Fig. 3c, d).
Also, a major German health insurance company demonstrated in its cohort of adult-insured patients a 6.5% decrease in screening services overall and in particular a 9% decrease in billed mammographies of the years 2019 and 2020 [17]. Similar results were shown by a study which surveyed 479,248 women in the USA, with a 6% decrease in mammography screening [18]. After the suspension of the mammography screening health professionals expected a rebound effect which started after May 2020 and was documented in a meta-analysis by Teglia et al. [8]. The authors describe an overall global screening decrease of 46.7% (with a maximum decrease of −67.7% in Europe) during April 2020. After June, they found a decrease of −13%. Besides, in a Dutch study focusing on women aged between 50 years and 74 years, breast cancer screening numbers started reaching the expected values at the end of 2020. This slight to moderate rebound highlights a recovery of cancer screening and diagnostic services starting in 2020 after the lockdown [19]. Annual reports published by two German statutory health insurance institutes indicate a slightly decreased screening participation in 2022 of about −10% compared to 2019 [10, 16, 17].
Data for breast cancer incidences in Germany from 2021 or more recently remain scarce. We conducted an analysis utilizing official cancer registries from three German states, focusing on breast cancer incidence rates for 2019 and 2021 (as depicted in Fig. 4) [20‒22]. Our examination revealed a decline in all three states during 2020 (Fig. 4a). Specifically, breast cancer incidences exhibited a slight decrease in two states at −5% and −3%, while one state experienced a more substantial reduction of −14% (Fig. 4b) compared to 2019. In 2021, incidences increased in two of the three states compared to 2019, but state 2 showed an elevated incidence rate compared to that in 2019 (Fig. 4b).
Genetic Screening Programs in High-Risk Patients
Especially BRCA1/2 mutation carriers benefit from early detection programs. The intensified early detection with additional mammary magnetic resonance imaging helps detect stage 1 tumors with reduced chemotherapy treatment. However, medical laboratories have been switched to SARS-CoV-2 virus diagnostics as part of the COVID pandemic. Expert personnel from the predictive field were frequently reassigned to support virus diagnostics. This resulted in a reduction of BRCA testing and delayed predictive gene mutation analysis for at least March–April 2020, which did not increase significantly after the lockdown phase and stayed apparent in 2020 [23, 24]. The COVID pandemic with the preservation of resources in health sectors resulted in a suspension and delay of testing potential mutation carriers with a decrease of up to 60% of genetic testing in core genes and did not recover after the lockdown phase in 2020. Suboptimal cancer treatment and risk management of patients with BRAC1/2 mutations could be the consequence of missed or unavailable genetic testing [23, 24]. Screening deficits are not completely compensated. Particularly alarming is the fact that elderly people over 50 years, with migration background or low socioeconomic factors are especially affected by a lack of early detection measures. Elderly and socially disadvantaged population groups in particular no longer participate in early detection programs [10, 14].
Diagnosis and Stage Shift
Consequently, there was a significant decrease in early breast cancer diagnoses [25]. A 10% decrease in small usually not palpable first-stage breast cancer diagnosis was reported in the Austrian National Cancer Register. A drop in the breast cancer diagnosis rate was about 18–29% was reported in a meta-analysis by Ng and Hamilton [26].
In terms of delayed diagnostics, a 2-month delay in secondary care could lead to a loss of lifetime: Sud et al. [27] referred to a 2 week-delayed diagnosis and extrapolated a diagnostic delay of 2 months without further effects of the COVID pandemic. Based on their model, there was a possible loss of lifetime of up to 0.7 years per patient (depending on age and tumor type), over the next 10 years [27].
A slight stage shift was visible in European collectives. An Italian single-center study documented a significantly lower proportion of in situ breast cancer diagnosis (stage 0–1/I–II, or Tis and T1; −10.4%) and an increase in node-positive (+11.2%) and stage III breast cancer (+10.3%) during the pandemic compared to the pre-pandemic period [28]. Similar observations were described in a French study: symptom-based breast cancer diagnosis significantly increased (86% vs. 57%). In particular, the detection rate of small tumors (T1) dropped by 38% and advanced cancers (T3, T4) increased by 80% [29]. This observation is also confirmed from a global perspective by Li et al. [1]: the majority of studies are describing a lower proportion of early stages and an increased proportion of advanced stages for breast cancer diagnosis during the pandemic. This further emphasizes that the disruption of mammographic screening is one factor for the visible stage shift in breast cancer diagnosis.
Psycho-Oncological Care
The pandemic also led to a sense of isolation and decreased social support, as well as increased psychological distress in oncological patients (Table 1). A significant limitation was observed in outpatient psycho-oncology (−12%) and follow-up (−21%) treatment during COVID pandemic [5]. The significance of the long-term survival of patients remains unclear. A survey conducted by the German Cancer Research Center interviewed 621 cancer patients, achieving a response rate of 34%. One-third of breast cancer patients reported (strong) worries related to COVID-19 infection or dying by coronavirus infection. Overall, the results indicated a significantly increased rate of depression, at +39%, and anxiety, at +55%, as measured by the HADS-A questionnaire [30]. Many patients describe that the pandemic, in particular, made their disease situation worse. Cancer-associated anxiety and pandemic-related stressors were multipliers of anxiety and depression associated with malignancies [31‒34]. Particularly, the highest level of anxiety related to the fear of COVID-19 was observed in patients with breast cancer, showing a rate of 20.67 ± 7.78. This was compared with genitourinary cancers at 17.63 ± 8.75, gastrointestinal cancer at 17.99 ± 6.79, and also higher than patients with lung cancers, showing a rate of 15.75 ± 5.92, as measured using the “Fear of COVID-19 Scale” (SRA-FCV-19S) [35]. Interestingly, patients with breast cancer awaiting delayed cancer surgery reported lower satisfaction with communication from oncology providers but overall did not seem to report more psychosocial difficulties than those who already had surgery [31]. Two studies by Schwab et al. [36] describe that a breast cancer history was an independent risk factor for worries about a more severe COVID-19 disease and also increased sorrow for a worse oncological outcome triggered by a COVID-19 infection [36, 37]. Accentuated worrying and higher levels of post-traumatic stress disorder were observed in employed cancer patients (47.4%) or women with cancer (27.9%) [38].
Cancer-associated anxiety . | Pandemic-related stressors . | Multipliers of anxiety and depression . |
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Cancer-associated anxiety . | Pandemic-related stressors . | Multipliers of anxiety and depression . |
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Inpatient Care Sector
General considerations how the COVID-19 pandemic has impacted the inpatient care sector of breast cancer patients is primarily the compensatory effort of all departments of the hospital to support the care for a rising number of people infected with the SARS-CoV-2 Virus. Primarily the intensive- and intermediate-care capacities of hospitals were shifted toward caring for the severe cases of COVID-19. Additionally, medical personnel were infected with the disease and were therefore sometimes missing an extended period of time. Furthermore, wards caring for breast cancer patients had to support intensive- and intermediate-care wards by lending personnel [3, 4]. All those factors led at least to some extent to a postponement of surgeries, reduction in the radicality of surgeries to prevent a needed intensive care unit (ICU) admission and might have led to a shift toward alternative treatment modalities (radiotherapy, neoadjuvant chemotherapy, oral therapies) [39, 40].
Amount of Breast Cancer Surgeries
The management of early breast cancer is built around the surgical care for the malignancy. To assess, the decline in breast cancer surgeries, the study group around Cairns, has compared the number of surgical procedures performed in 2019 and 2020 and found no decline in the overall volume of operations since the beginning of the COVID-19 pandemic. Even though they have seen a short-term decline in screening and diagnostic mammograms during the same time period, there was no significant difference in breast cancer stage at the time of operation [41]. The German Cancer Research Center (Deutsches Krebsforschungszentrum [DKFZ]) has evaluated the oncological capacities during the time March 2020–June 2022 of 18 comprehensive cancer centers in Germany and has seen a total decline of breast cancer surgeries of 9% (compared to before March/2020), whereas in other international studies, a decline in surgical capacities of 10% has been labeled as relevant [5].
A German survey conducted in 18 comprehensive cancer centers with a total of 621 patients analyzed, investigated whether the pandemic had any effect on those patients’ cancer care. In this study, which included 76% female patients with the predominant malignancy being breast cancer (50% of total patients), 12.9% of patients reported that there was any change in cancer care. Regarding the surgical and systemic treatments 1.6% and 2.3%, respectively, reported any change in their therapeutic modalities which in most of the cases meant a postponement [42]. An international, prospective cohort study published by the COVIDSurg Collaborative in 2021 evaluated the effect of the COVID-19 pandemic lockdowns on planned cancer surgery for 15 different tumor types. In their analyses, they did not see a significant surgical delay for breast cancer, whereas for the majority of other malignancies, there was a delay to some extent evident. They have shown that every seventh patient did not receive their surgery during a full lockdown due to pandemic-related reasons [43]. Also, a German study, comparing the data of a large statutory insurance agency from 2019 with 2020, has not seen a decrease in surgeries during the periods of the German lockdown in March and April of 2020, compared to the respective months in 2019. On the contrary, even an increase of 5% regarding surgeries for breast cancer was shown. One of the reasons for said increase was a reported tendency to omit treatment with neoadjuvant chemotherapy and therefore reduce the number of immunocompromised patients during the COVID-19 pandemic [17, 44]. Similar findings were reported in a meta-analysis of 24 studies conducted by de Bock et al. [45], who examined the impact of guidelines on surgical oncology during the pandemic. Surgical procedures in the oncological pathway decreased (−26.4%). However, the authors observed a slight increase (0.3%) for breast cancer surgery procedures. This was attributed to the availability of vacant operating time slots due to a drastic postponement of elective benign surgical cases that could be easily filled by breast cancer procedures and were prioritized to a greater extent. This could be associated with the fact that patients undergoing such procedures tend to have shorter postoperative hospital stays and a reduced need for intensive care unit admission compared to other oncological surgery cases. The same study reported no difference in the number of postoperative complications during the pandemic [45]. Another reason for a non-significant delay from diagnosis to surgery in most of the studies was an increased use of regional anesthesia instead of general anesthesia compared to the pre-pandemic period. This could have also been a reason for increased same-day discharges [46‒49]. Nevertheless, some studies still reported a significant delay from diagnosis to surgery for primary breast cancer. The international survey conducted in 24 countries analyzing the impact of COVID-19 on breast cancer management, published by Mathelin et al. [50] found a delay in surgery particularly in the population of frail patients who were at increased risk when they contracted the SARS-CoV-2 virus. This population was increasingly treated with a neoadjuvant endocrine therapy, which went from being rarely prescribed to being frequently prescribed during the pandemic [50]. In addition, the ESMO recommendations for breast cancer management in the COVID-19 era suggested that clinically low-risk breast cancer cases were of medium priority for surgery and could be considered for neoadjuvant endocrine therapy, explaining the delay in surgery in some studies [51].
Impact on Breast Reconstruction Surgeries
Most published articles state that there definitely was an influence of the COVID-19 outbreak on the mode and timing of breast reconstruction. According to Fancellu et al. [47], patients were less likely to receive immediate breast reconstruction at the time of breast cancer surgery at the height of the pandemic. In addition, Rubenstein and colleagues [52] reported that, while overall reconstruction rates remained unchanged during the pandemic, the percentage of tissue expander reconstruction increased (from 64.0 to 68.4%), while autologous and direct-to-implant reconstruction decreased during the pandemic (15.2–13.4% and 20.7–18.2%, respectively) [52]. Another study published by Joseph et al. [53], which surveyed plastic surgeons in the USA and received responses from 223 surgeons, found that 19.0% of surgeons did not offer immediate breast reconstruction at the height of the pandemic and that 47.7% did not offer autologous/flap reconstruction methods. Similarly, a systematic review by Hemal and colleagues [54] showed that autologous breast reconstruction was delayed during the pandemic to conserve resources, due to longer operative time and a longer hospital stay. They also described a reduction in immediate breast reconstruction at the peak of the pandemic, although this was resumed after the peak because of its superiority to delayed breast reconstruction, e.g., to reduce exposure to COVID-19 [54].
Shift in Treatment Modalities?
The pandemic forces clinicians to modify guidelines which recommend treatment changes to balance the risk of a COVID-19 infection with disease progression. Comparing these data internationally, a large population-based retrospective study in the USA has seen a marked shift toward the use of neoadjuvant chemotherapy (12% vs. 38%) as well as neoadjuvant endocrine therapy (5% vs. 27%) during the first 2 months of the COVID-19 pandemic. Those changes did not persist and returned to the pre-pandemic distribution of treatment modalities [2, 55]. Similarly, a multicenter study in Austria including 18 centers and 552 patients with breast cancer has seen a proportional increase in neoadjuvant chemotherapy of 18%, corresponding to a decrease in surgical therapy during the months of lockdown (March 2020–May 2020) compared to the pre-pandemic levels [25]. Furthermore, a Dutch population-based study of almost 34,000 women with breast cancer documented a 339% increase in neoadjuvant endocrine therapy during the lockdown. On the contrary, neoadjuvant chemotherapy was less likely (up to 44% reduction) for stage I/II and hormone receptor+/HER2-tumors diagnosed during transition compared to 2019 [39].
Impact on Activity of Clinical Trials
Also, the clinical trial activity was impacted by the COVID-19 pandemic. Early during the pandemic, the initiation of new clinical trials on cancer and patient enrollment was severely disrupted by −46 to −57% in the USA. This decline likely reflects a diversion of resources toward immediate patient care during the pandemic. For non-US-based studies, the drop was less dramatic with an overall reduction of 27%. Nevertheless, the initial decline recovered progressively and eventually reached pre-pandemic levels [4, 56‒58]. According to a study by Fleury et al., cancer survivors were asked about their attitudes toward trial participation during the COVID-19 pandemic. 20% of patients with cancer indicated they would be less willing to participate in a clinical trial owing to fears about contracting COVID-19, due to a possible infection risk while staying at clinics for therapy [59].
Discussion
The COVID-19 pandemic has presented significant challenges for breast cancer care and patients, with several key areas of impact emerging from the literature. These include screening, diagnosis, therapy, inpatient care, aftercare, and the psychological well-being of patients.
The pandemic has disrupted routine breast cancer screenings, resulting in potential delays in early detection (majority of studies at least 49%) and subsequent treatment initiation (18–29%) [1, 26]. Limited access to diagnostic procedures has also led to delayed or missed diagnoses, further complicating patient care. However, studies have shown that breast surgeries remained stable during the first wave of the pandemic [45], suggesting that the negative effects on medical healthcare were not as strong as initially thought. Effects on prognosis are likely to be primarily due to delayed diagnosis, resulting maybe in a small long-term effect.
Nevertheless, in Germany, most breast cancer patients received treatment within an appropriate time frame, but the effects of reduced follow-up are yet to be estimated. Many effects will only be answered in a larger time frame with the help of cancer registries.
The screening programs experienced the largest drop during the lockdown, with a decrease of −67% in Europe and −35% in North America. After the lockdown, breast cancer screening started to recover slightly, with a rebound effect becoming noticeable at the end of 2020 and during 2021 [8]. However, screening recalls remain crucial due to persistent reluctance for screening visits, also in Germany [16]. The disruption of mammographic screening is one factor for the visible stage shift in breast cancer diagnosis. It stressed the importance to recall persistently for the screening measures. It is still too early to know if delayed screening during the pandemic will lead to higher breast cancer morbidity and mortality. First insights from the German perspective suggest a potentially low pandemic effect on breast cancer incidences, which might not necessarily be accurate. The available data spanning 2019–2021 or newer underscore the challenge of deducing a long-term effect.
It is important to emphasize that elderly individuals over 50 years, those with a migration background or those with low socioeconomic status are especially affected by lack of early detection measures. These results suggest that recall systems need to focus on these groups in the future. Recalls for early detection measures need to be intensified and transitional extension of age limits need to be discussed. Polities should focus on identifying any underlying cultural barriers to ensure a return to routine care.
Surprisingly, the effects of delayed BRCA testing during the COVID-19 pandemic have been poorly reported with few existing studies [23, 24]. Further retrospective studies are needed, as a delay in testing for this high-risk population could result in a backlash against successful early detection programs and needs to be closely monitored in the future.
Most published studies have not reported a significant decrease in surgical procedures and inpatient breast cancer care was able to be maintained during the pandemic. Modified surgical pathways did not significantly affect the morbidity and mortality rates compared to the pre-pandemic period. Although some studies have noted an increased use of neoadjuvant chemotherapy, no treatment delays were evident [43, 60].
Furthermore, the disruption of clinical trials was short-lived, and it is unlikely to significantly slow down the pace of clinical research and development of new drugs [4, 56, 57]. While there was a noticeable impact on the volume of surgical oncology, it did not significantly affect the clinical oncological outcomes. The frequency of surgical breast cancer procedures remained stable during the pandemic [45].
Different modeling studies exist and should be considered carefully [27, 61‒65]. The prediction models for the COVID-19 impact on medical care display a wide range of increased numbers for breast cancer cases and/or increased mortality rates. However, it is important to note that real-life situations cannot be completely captured by these scenarios and different countries implemented different strategies to manage the pandemic, which were also adjusted over time [1]. Prediction of the clinical outcomes without more data remains difficult in 2023.
German cancer registries are providing the first nationwide insights, which are indicating that the impact on breast cancer incidence and mortality could be lower than expected, resulting in a small long-term effect [5, 16, 17, 44]. However, the biggest impact on cancer patients was observed at the national, European, and international levels in terms of follow-up and psychosocial care. The resulting effects on cancer patients are under examination and remain to be fully understood. The impact of the pandemic on psychologic health, prognosis and treatment should be an essential part of the medical conversation with the patient [4, 31‒33, 36, 38].
Isolation, fear of contracting the virus, treatment uncertainties, and reduced social support led to heightened stress levels and mental health concerns among this vulnerable population [66]. Especially, the lack of supportive networks, support groups, and the reduced communication with medical and nursing staff during the COVID-19 pandemic magnified the depression and anxiety of cancer patients [66, 67]. This needs to be addressed through national health promotion programs, which should identify the needs of patients [68]. Implementation of telehealth services or screening calls for anxiety and depression via telephone could make an important contribution in the future [32]. Approaches for this have already been tested thanks to the exceptional situation in 2019 but must be further developed and adopted in regular care [69]. Rural areas or immobilized patients could benefit from this in particular [70].
The COVID-19 pandemic posed significant challenges to healthcare systems worldwide, but it also led to several positive developments in breast cancer care. A study by McKinsey [71] found that the pandemic accelerated digital transformation by 7 years, reflecting the increased adoption of telemedicine. This facilitated virtual consultations and remote monitoring for breast cancer patients, enhancing access to care and continuous patient support. This ensured continuous care while minimizing infection risks. Studies indicate that patients with higher socioeconomic status particularly took advantage of these technologies [72‒74].
Additionally, the pandemic spurred the rapid implementation of minimally invasive techniques and outpatient treatment options, reducing hospital stays and infection risks, thereby enhancing the efficiency and safety of breast cancer [75, 76]. The necessity for a coordinated response to the pandemic also strengthened interdisciplinary collaboration between various medical fields and institutions, leading to better coordination and integration in breast cancer care, supported by enhanced networks and knowledge-sharing platforms [77]. Moreover, the pandemic highlighted the importance of patient-centered care, with increased efforts to prioritize the needs and preferences of patients. Patients reported high satisfaction with using telemedicine to communicate with their oncologists, underscoring the significance of a patient-focused approach [72, 74]. The crisis required swift adjustments in processes and workflows, resulting in efficiency improvements in breast cancer care. More flexible appointment scheduling and the possibility of conducting certain treatments at home contributed to a more patient-friendly care environment [77, 78]. These advancements demonstrate that despite the challenges posed by the pandemic, some positive changes and innovations in breast cancer care emerged, which may have lasting benefits and further improve care delivery.
Conclusion
Based on this literature review, we have found that the impact on breast cancer care was unexpectedly not as significant as predicted. The redesigned guidelines and modifications in medical and/or oncological healthcare, which were enforced due to the pandemic, were successfully implemented in clinical settings by healthcare professionals. Especially in the context of breast cancer care, early signs indicate a better outcome than initially feared during the acute phase of the pandemic. However, quantifying the consequences of the pandemic will require several years due to the delay in the dissemination of population-based surveillance data.
Nevertheless, the pandemic significantly affected the mental well-being of breast cancer patients. This underscores the importance of timely and effective communication of breast cancer management guidelines to alleviate the fears of the general public.
Statement of Ethics
This publication does not involve any trials or experiments conducted by the authors. The research presented in this article is based on a review and analysis of existing data and literature. An ethics statement was not required for this study type as it is based exclusively on published literature. The authors have adhered to ethical standards in reporting the information and have made every effort to ensure that all data sources and references are appropriately cited and credited.
Conflict of Interest Statement
The authors declare that they have no conflicts of interest related to this research. There are no financial, personal, or professional relationships that could be construed as influencing the work reported in this article.
Funding Sources
This research received no specific funding from any public, private, or commercial source. The study was conducted as part of the authors’ academic and professional responsibilities, and no external financial support was provided for this research.
Author Contributions
M.N. and M.P. substantially contributed to the conception and design of the work, conducted the screening and evaluation of retrieved titles, abstracts, and full-texts for inclusion, and were responsible for the acquisition, analysis, and interpretation of data for the work. They also played a pronounced role in drafting the work and reviewing it critically for important intellectual content. T.N.F. and B.B. provided essential guidance throughout the research process, helping resolve discrepancies during the screening and evaluation. They were instrumental in overseeing the study and data interpretation. Additional subject matter expertise was sought from co-authors F.D., N.K., J.-P.C, S.M., E.R., and E.C.S.-I. in specific areas. They provided valuable insights and field-specific input for data interpretation and research analyses. All authors and co-authors gave their final approval for the version to be published and agreed to be accountable for all aspects of the work, ensuring that questions related to the accuracy or integrity of any part of the work were appropriately investigated and resolved. The authors also have confidence in the integrity of each other’s contributions.
Additional Information
Maximilian Pruss and Melissa Neubacher contributed equally to this work.
Data Availability Statement
The data that support the findings of this study are openly available in reports of German official registry sites: Cancer Registry Schleswig-Holstein, data call on June 4, 2023 (https://www.krebsregister-sh.de/iWOB/index.html#/database/timeline); Cancer Registry Hamburg, data call on June 4, 2023 (https://interaktiverbericht.krebsregister-hamburg.de/#/diagnoses/overview); Annual Report Cancer Registry Thueringen, 2021, published 2022, data call on June 4, 2023 (https://cloud.krebsregister-thueringen.de/owncloud/index.php).