Research ArticleClinical Studies
Open Access

Impact of PEG-GCSF in Breast Cancer Patients Undergoing Chemotherapy During the COVID-19 Pandemic: Single Center Experience and Literature Review

KIOTO YOKOYAMA, NOBUYASU YOSHIMOTO, SATORU TAKAYAMA, MASAKI SAKAMOTO, KEISUKE TOMODA, KEN ISHIKAWA, MASAKATSU YAMASHITA, HIROTO SUZUKI, RYOSUKE HOSOGI, MASAHIRO TAKAHASHI, MARI FUKUDA and HISANORI KANI
In Vivo September 2024, 38 (5) 2335-2340; DOI: https://doi.org/10.21873/invivo.13699

Abstract

Background/Aim: The COVID-19 pandemic brought many challenges in healthcare systems globally. Pegylated granulocyte colony stimulating factor (PEG-GCSF) is recommended to reduce febrile neutropenia (FN), however there are a few reports that G-CSF might worsen COVID-19 disease, and its appropriate use during the COVID-19 pandemic remains uncertain. This retrospective study aimed to analyze the association between PEG-GCSF use and COVID-19 infection and severity. Patients and Methods: Breast cancer patients who received chemotherapy at the Nagoya Tokushukai General Hospital between October 2020 and April 2023 were included. Patients with suspected COVID-19 symptoms during each chemotherapy cycle underwent COVID-19 antigen testing. To assess the potential impact of PEG-GCSF on COVID-19 severity, we collected data on patient background, chemotherapy regimens, PEG-GCSF use, COVID-19 antigen tests, and COVID-19 infection from their medical records. Results: Thirty patients received chemotherapy. In total, 71 cycles were administered comprising adriamycin and cyclophosphamide (AC; 37 cycles), docetaxel (DTX; 26 cycles) and docetaxel and cyclophosphamide (TC; eight cycles). Among those patients, suspected COVID-19 symptoms were observed in only one of 62 cycles of the three regimens (1.6%) with PEG-GCSF compared to two of nine cycles (22.2%) without PEG-GCSF (p=0.0405). However, because none developed COVID-19 infection during chemotherapy, we could not assess COVID-19 severity and PEG-GCSF use. Conclusion: A potential role of PEG-GCSF in reducing suspected COVID-19 symptoms during chemotherapy, reducing the anxiety and need for hospital visits, thus improving patients’ quality of life, is suggested. These insights could contribute to optimizing the care of breast cancer patients in situations like the current pandemic.

Key Words:

Pneumonia caused by the novel coronavirus, Coronavirus Disease 2019 (COVID-19), was first reported in Wuhan, China in December 2019, and subsequently spread all over the world causing a pandemic (1). In Japan, the 10th wave is now developing, thus the pandemic continues. The COVID-19 pandemic has had a large impact on healthcare systems worldwide, including cancer treatments (2, 3). Breast cancer, one of the most significant malignancies among women globally, often necessitates the administration of chemotherapy with a relatively high risk of myelosuppressive effects and febrile neutropenia (FN) (4). The American Society of Clinical Oncology (ASCO) and European Society for Medical Oncology (ESMO) have issued guidelines recommending consideration of the prophylactic use of colony-stimulating growth factor during chemotherapy for patients at over 20% risk of developing FN (5, 6). However, a few reports have suggested a potential increase in the risk of worsening disease severity in COVID-19 patients with cancers who received granulocyte colony stimulating factor (G-CSF) (7, 8). Consequently, the specific implications of G-CSF use in cases of COVID-19 infection remain uncertain. Therefore, there is a need to clarify the usefulness and risk of G-CSF administration in breast cancer patients undergoing chemotherapy during the COVID-19 pandemic. We conducted a retrospective study at our hospital to gain insight into the association between use of G-CSF, especially pegylated granulocyte colony stimulating factor (PEG-GCSF), and COVID-19 infection incidence and severity in breast cancer patients receiving chemotherapy.

Patients and Methods

This retrospective study included breast cancer patients who underwent chemotherapy at our Hospital between October 2020 and April 2023. Electronic medical records were retrospectively reviewed to collect patients’ data, including chemotherapy regimens, use of PEG-GCSF, COVID-19 infection, and COVID-19 severity. The use of PEG-GCSF during chemotherapy cycles was also analyzed, with particular focus on patients receiving adriamycin and cyclophosphamide (AC), docetaxel (DTX), and docetaxel and cyclophosphamide (TC) regimens. When suspected COVID-19 symptoms arose during chemotherapy, COVID-19 antigen tests were conducted.

Furthermore, the proportion of cycles with suspected COVID-19 symptoms who underwent COVID-19 antigen testing was compared between the PEG-GCSF group and the non-PEG-GCSF group using Fisher’s exact test. Ethical considerations were addressed by ensuring compliance with the Declaration of Helsinki, and approval was obtained from the Tokushukai Group Ethics Committee (#TGE02062-016).

Results

A total of 30 patients (including three cases of bilateral breast cancer) received chemotherapy during the study period. Among them, 29 patients (96.7%) were female sex, and one patient (3.3%) was male. The median age of the patients was 58 years, ranging from 34 to 80 years. Sixteen patients (53.3%) were diagnosed with early breast cancer, while 15 patients (50.0%) had advanced or recurrent breast cancer. One patient initially diagnosed with early breast cancer developed recurrent breast cancer during the study period. Regarding the biological features of breast cancer, 22 cases (66.7%) were estrogen receptor (ER) positive, while 11 cases (33.3%) were ER negative. In terms of progesterone receptor (PgR) status, 18 cases (54.5%) were positive, and 15 cases (45.5%) were negative. Seven cases (21.2%) were human epidermal growth factor receptor 2 (HER2) positive, whereas 26 cases (78.8%) were HER2 negative. Three patients (10.0%) had suspected COVID-19 symptoms, however there was no COVID-19 infection during the period of this study (Table I). The most commonly used chemotherapy regimens were as follows; 10 patients (33.3%) received AC, seven patients (23.3%) received DTX, two patients (6.7%) received TC, four patients (13.3%) received dose-dense AC, 12 patients (40.0%) received weekly paclitaxel (wPTX) and nine patients (30.0%) received the oral anticancer medication S-1. Anti-HER2 drugs, anti-vascular endothelial cell growth factor (VEGF) drugs and immune checkpoint inhibitors were not included in this analysis of chemotherapy regimens as they do not affect white blood cells (Table II). Considering the cumulative number of cycles, AC was administered for a total of 37 cycles, DTX for 26 cycles, and TC for 8 cycles (Table III). There were only two patients who were not administered PEG-GCSF in every chemotherapy cycle, one patient who received DTX for four cycles, but PEG-GCSF was only given in three cycles, and another patient who received both AC and DTX for four cycles each but did not receive PEG-GCSF at all during chemotherapy. There were three instances where COVID-19 was suspected, leading to the administration of COVID-19 antigen tests. However, all tests were negative, so no cases of COVID-19 infection were observed among the patients in this study. The PEG-GCSF group included 33 (89.2%) cycles of AC, 21 (81.5%) cycles of DTX and eight (100%) cycles of TC, while the non-PEG-GCSF group included four (10.8%) cycles of AC, five (18.5%) cycles of DTX, and no cycles of TC (Table IV). Comparing the PEG-GCSF group (62 cycles) to the non-PEG-GCSF group (nine cycles) among the total of 71 cycles of AC, DTX and TC regimens, a significantly lower proportion of patients with suspected COVID-19 symptoms underwent antigen testing in the PEG-GCSF group compared to the non-PEG-GCSF group [one (1.6%) vs. two (22.2%), p=0.0405*, Fisher’s exact probability test] (Table V). In this study, we did not find any cases of COVID-19 infection among breast cancer patients undergoing chemotherapy, so we could not analyze the relationship between G-CSF use and COVID-19 infection severity.

View this table:
Table I.

Patient characteristics.

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Table II.

Regimens administered during the study period.

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Table III.

Number of cycles administered for the AC, DTX, and TC regimens.

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Table IV.

Administration of PEG-GCSF for the AC, DTX, and TC regimens.

View this table:
Table V.

Relationship between PEG-GCSF administration and suspected COVID-19 symptoms in the AC, DTX, and TC regimens (total 71 cycles).

Discussion

At our Institution we routinely used PEG-GCSF for breast cancer chemotherapy patients, but at the beginning of the pandemic we believed that PEG-GCSF use could somehow reduce the risk of COVID-19 infection because we did not have enough experience and knowledge. Since then, there have been few findings about COVID-19 and cancer chemotherapies.

Cancer patients undergoing treatment have been reported to be susceptible to COVID-19 and to be at higher risk of severe illness due to their compromised immune systems (9, 10). Furthermore, studies suggested that the mortality rate of COVID-19 in younger, lung and hematologic cancer patients was higher, but by diagnosing COVID-19 earlier its mortality rate could be improved (11, 12). COVID-19 causes not only physical problems but also mental distress, with some reports indicating an inverse correlation between psychological well-being and COVID-19-related anxiety in cancer patients (13-16).

Myelosuppressive effects and FN are common complications of cancer chemotherapy, carrying a potential threat to life (6, 17, 18). Primary prophylactic administration of G-CSF is widely recognized to notably reduce FN incidence and infection frequency (19-22). One interesting report about G-CSF in the COVID-19 pandemic concluded that it is better to lower the threshold for G-CSF treatment, expanding prophylactic G-CSF use to all patients with a more than 10% risk of FN, to reduce exposure to the virus (23). Now major societies, such as the ASCO, the ESMO and the National Comprehensive Cancer Network (NCCN) have updated guidance on G-CSF use to expand its indication for more than 10% risk of FN (24-26), and similarly, the Japanese Breast Cancer Society now recommend active use of PEG-GCSF to reduce the risk of FN (27). Since in Japan the COVID-19 pandemic still continues, with a 10th wave beginning in November 2023, we now continue active use of PEG-GCSF. On the other hand, Grazia et al. use G-CSF to enhance chemotherapy strength in the firstly place (28), and Suzuki et al. use G-CSF secondary for patients who occurred FN during TC (29).

However, one notable study reported that G-CSF administration may lead to worsening clinical and respiratory status (7), and furthermore the respiratory status of a patient with metastatic breast cancer who contracted COVID-19 reportedly worsened after she was given two doses of filgrastim to treat neutropenia (30). PEG-GCSF treatment carries the possible side effect of angiitis, and this mechanism might be related to these symptoms. This was the main incentive for us to conduct this retrospective study.

There is currently no clear evidence on the impact of G-CSF, which affects the immune system, on the COVID-19 pandemic. The ASCO justifies the prophylactic use of highly-myelosuppressive immunotherapy to prevent neutropenia or myelosuppression, which could potentially increase the risk of COVID-19 infection as described above.

Additionally, for known cases of neutropenic fever, it is recommended to perform rapid testing for COVID-19, when available, to determine the appropriate level of personal protective equipment (PPE) required for caregivers and to identify suitable locations within the healthcare facility to continue care (24). The NCCN has expanded its recommendation for the routine prophylactic use of G-CSF to consider the increased risk associated with excessive exposure to healthcare environments, such as emergency centers and outpatient clinics during a pandemic (26). A recent study indicated a potential increased risk of acute respiratory distress syndrome (ARDS) associated with G-CSF administration during chemotherapy. Zhang et al. noted that, considering the significant influx of neutrophils into the lungs as a hallmark of ARDS, administering G-CSF to all COVID-19 patients may have detrimental consequences (7). In terms of this point, the ESMO recommends considering an expansion of the indications for post-chemotherapy G-CSF to reduce the risk of FN as above, based on the need to minimize outpatient visits and emergency department visits to decrease the risk of COVID-19 infection while acknowledging the concern that the risk of ARDS associated with COVID-19 may not outweigh the benefits of reducing FN risk (25).

One of the main objectives of the study was to investigate the association between PEG-GCSF use and COVID-19 severity in breast cancer patients undergoing chemotherapy. The study participants comprised breast cancer patients who received chemotherapy between October 2020 and April 2023. However, notably none of the patients included in the study developed COVID-19 infection during the chemotherapy period, thus no assessment of COVID-19 severity could be carried out. An interesting observation in this study was the significantly lower proportion of cycles with suspected COVID-19 symptoms who underwent antigen testing in the PEG-GCSF group compared to the non-use group. This suggests a potential reduction in the incidence of COVID-19-related symptoms during chemotherapy with the administration of PEG-GCSF. We think it was one reason that PEG-GCSF can reduce febrile neutropenia with high fever that was also typical symptom of COVID-19, so patients in the PEG-GCSF group did not need receive COVID-19 antigen tests so much to distinguish COVID-19 or FN. For cancer patients with high levels of anxiety related to COVID-19, mitigating these symptoms could provide significant benefits to the patients’ mental health. Additionally, reducing the occurrence of COVID-19-related symptoms may lead to fewer outpatient visits and potentially reduce the risk of COVID-19 exposure.

The major limitation of this study is that the sample size was relatively small, particularly in terms of patients who did not receive PEG-GCSF. Among the patients who received AC, DTX, and TC regimens, only two patients did not receive PEG-GCSF. Larger sample sizes, randomized designs, and a focus on respiratory outcomes are necessary for future research to enhance the comprehension of the safety profile and potential risks linked to PEG-GCSF use during chemotherapy. Such insights could be beneficial not only in the present circumstances of the global COVID-19 pandemic, but also in anticipation of potential future pandemics.

Conclusion

This study suggests a potential alleviating effect of PEG-GCSF use on suspected COVID-19 symptoms. While constrained by a small sample size and retrospective design, the results showed the usefulness of PEG-GCSF during the COVID-19 pandemic. Larger, randomized studies are required to more comprehensively assess the safety of PEG-GCSF during chemotherapy. This understanding could enhance the care of breast cancer patients in both current and future pandemic scenarios of other infectious diseases.

Footnotes

  • Authors’ Contributions

    Research design: Yokoyama K, Yoshimoto N, collection and analysis of data: Yokoyama K, Yoshimoto N; all Authors contributed to reviewing the article. All Authors read and approved the final article.

  • Conflicts of Interest

    The Authors report no conflicts of interest related to this study.

  • Received May 2, 2024.
  • Revision received May 30, 2024.
  • Accepted June 11, 2024.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

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Impact of PEG-GCSF in Breast Cancer Patients Undergoing Chemotherapy During the COVID-19 Pandemic: Single Center Experience and Literature Review
KIOTO YOKOYAMA, NOBUYASU YOSHIMOTO, SATORU TAKAYAMA, MASAKI SAKAMOTO, KEISUKE TOMODA, KEN ISHIKAWA, MASAKATSU YAMASHITA, HIROTO SUZUKI, RYOSUKE HOSOGI, MASAHIRO TAKAHASHI, MARI FUKUDA, HISANORI KANI
In Vivo Sep 2024, 38 (5) 2335-2340; DOI: 10.21873/invivo.13699
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