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Opportunities and challenges encountered in managing cervical cancer during the coronavirus disease 2019 pandemic

Infectious Agents and Cancer volume 19, Article number: 41 (2024) Cite this article

Abstract

Objectives

The COVID-19 pandemic, while putting pressure on the global healthcare system, has had a significant impact on the prevention, diagnosis, and treatment of cervical cancer. The aim of this study is to provide an overview of the challenges and opportunities presented to cervical cancer during the COVID-19 pandemic and to provide lessons for better coping with cervical cancer in future pandemics.

Methods

The search terms included the following: SARS-CoV-2 and/or COVID-19 with cervical cancer and HPV. The initial literature search began on June 1, 2022 and ended on March 1, 2023.

Outcome

COVID-19 has hindered the cervical cancer screening, delayed the diagnosis and treatment of cervical cancer, increased the public’s anxiety, and negatively affected the management of cervical cancer. However, the occurrence of COVID-19 pandemic has promoted the development of new human papillomavirus (HPV) tests and improved the rates of HPV self-sampling, offering a small window of opportunity to eliminate cervical cancer.

Conclusions

In the next few years, the COVID-19 pandemic will come to an end, and the eradication of cervical cancer should always be carried out. We should draw lessons and experience from this global pandemic, and make efforts for the subsequent eradication of cervical cancer.

Introduction

It has been more than 3 years since the coronavirus disease 2019 (COVID-19), a lung disease caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), was declared as a pandemic. The virulence of the novel coronavirus variant has been greatly reduced, but it remains a global concern and poses a major challenge to the global healthcare system [1]. In the previous COVID-19 pandemic, caring for and treating COVID-19 patients have been a major goal of most countries; however, this may have affected other priorities of the global healthcare system, such as cancer treatment and screening, and may even have delayed the identification and diagnosis of cancer patients, thus affecting their survival [2,3,4,5]. As one of the three major types of gynecological cancers, several aspects of cervical cancer have been greatly affected by the current pandemic: vaccination, screening, diagnosis, and treatment; the pandemic also caused emotional and psychological pressure among this patient group. Although the COVID-19 pandemic has negatively affected the efforts of the World Health Organization (WHO) to eliminate cervical cancer, some new HPV detection strategies have been developed based on the COVID-19 detection method, making it possible for people to detect HPV at home. If this method is promoted, the detection of HPV will be improved further. This is an opportunity that the past COVID-19 pandemic has given to eliminate cervical cancer. This review aimed to address the opportunities and challenges faced by cervical cancer patients during the COVID-19 pandemic, as shown in Fig. 1.

Fig. 1
figure 1

The summary of the effects of COVID-19 on cervical cancer

Full size image

Results

Effect of COVID-19 in cervical cancer screening

After the COVID-19 pandemic, many countries and regions have reduced or even discontinued cancer screening, including cervical cancer screening [6,7,8]. The COVID-19 pandemic has exposed the lack of pharmaceutical products, personal protective equipment, and diagnostic supplies worldwide [9]. This has undoubtedly impacted the implementation of cervical cancer screening programs, with up to 74% of the 57 HPV DNA testing laboratories from 30 countries reporting the lack of supplies and staffing shortages (54%) [10]. According to the study conducted by Shen et al. [11], during the COVID-19 pandemic in the United States, the cervical cancer screening rate decreased by 80–90%; in Taiwan and China, the cervical cancer screening rate decreased by 15–40%. Although the American Cancer Society has stated that cancer screening during the COVID-19 pandemic is still important, the decline in cervical cancer screening rates is inevitable. Similar results have been observed worldwide, with Poland reporting a cervical cancer screening rate of 17% among women in 2020 as a result of the COVID-19 pandemic [12]. The number of samples accepted by the United Kingdom laboratories responsible for HPV screening also decreased significantly from April to June 2020, and approximately 70% of women were forced to delay cervical cancer screening [13]. Castanon et al. [13] estimated that of the 146,391 women whose next scheduled screening was postponed due to the COVID-19 pandemic, an additional 60 cases of cancer were expected to occur. Compared with developed countries, the cervical cancer screening rate in low-income countries is adversely affected [14]. In low-income countries, the medical resources are relatively scarce, and the COVID pandemic has increased the tension on medical resources. Cervical cancer screening and other non-essential health services have been temporarily suspended to prioritize the care of symptomatic COVID-19 patients. According to the COVID-19 and the Cancer Global Modeling Alliance, interruptions in cervical cancer screening associated with the COVID-19 pandemic will increase the cancer burden in women aged below 50 years by 5% and 6% [15]. Due to low income, ethnicity, remoteness of residence, and gender, these unserved people have experienced differences in cancer screening and management in the current pandemic, and social and healthcare-related inequalities caused by COVID are further exacerbating [16]. In addition to the obvious reduction in screening rates due to the strain on health resources in the current pandemic, the impact of a decline in patient’s interest in undergoing preventive screening cannot be ignored. A 2020 study that examined the number of Google searches for the term “pap smear” showed a 54.1% decrease in the use of these search terms compared with that in the same period prior to the pandemic [17]. Although the COVID-19 pandemic has caused difficulties in the implementation of cervical cancer prevention measures, the corresponding response measures are constantly being promoted. Of course, the impact of COVID-19 on cervical cancer screening will also be short-lived, as these screening services resume soon after the pandemic.

COVID-19 pandemic causing great difficulties to the vaccination of HPV

HPV is the most important cause of cervical cancer; therefore, the primary preventive measure against cervical cancer is HPV vaccination [18, 19]. Prior to the COVID-19 pandemic, countries worldwide have been promoting cervical cancer vaccination to prevent cervical cancer. The WHO also has a strategy to accelerate the elimination of cervical cancer, and 200 million doses of HPV vaccine were administered worldwide by 2020 [20, 21]. In the COVID-19 pandemic era, the realization of this strategy has become a major challenge. Compared with that in 2019, the global annual dose of the HPV vaccine was reduced by 24% in 2020 [12]. A gap in global vaccination rates is not expected to occur until 2031 [22, 23]. However, an analysis of Google searches shows that since the beginning of the pandemic, the level of interest in HPV vaccination has remained unchanged compared with that prior to the COVID-19 pandemic [24]. Although the COVID-19 pandemic reduced the people’s enthusiasm to undergo cervical screening, it did not dampen their enthusiasm for HPV vaccination. However, due to the shortage of health resources caused by the pandemic, interruption of the vaccine supply chain, and deterioration of the country’s financial health status, cervical cancer vaccination has been affected to a certain extent [25,26,27,28]. The coverage rate of HPV vaccine in rural areas is 10% lower than that in urban areas, which is caused by a number of factors, including low public awareness, reduced interest of medical staff in carrying out prevention activities, and limited number of outlets providing medical services [29]. In many countries worldwide, a large proportion of the population lives in rural areas; therefore, essential methods to promote HPV vaccination in these areas should be developed. The COVID-19 pandemic has caused great difficulties in implementing cervical cancer vaccination. To overcome this difficult period and complete the WHO strategic plan to eliminate cervical cancer, funded by governments of various countries, the implementation of national free HPV vaccination is an effective method.

COVID-19 pandemic adversely affecting the treatment of cervical cancer patients

The novel coronavirus pandemic not only has an indelible impact on the prevention of cervical cancer but also affects the choice of surgical method for cervical cancer patients, which has a negative effect on the treatment of cervical cancer patients [30]. However, the impact of COVID-19 on cervical cancer patients is more focused on the longer waiting period for surgery and the delays in treatment than on the change in surgical methods.

Physical isolation, travel restrictions, and reduced public transport facilities (including roads, railways, and airports) owing to the COVID-19 pandemic have made it difficult for patients to reach hospitals for treatment. Second, during the COVID-19 pandemic, patients are worried about contracting COVID-19 while staying in healthcare facilities, which further discourages them from seeking medical attention [31]. In addition, most hospitals have discontinued performing some non-essential surgical procedures and postponed the provision of some non-essential services during the COVID-19 pandemic [32, 33]. All of these factors have led to a serious delay in the completion of treatment for cervical cancer patients, thus decreasing their survival rate. In the current COVID-19 pandemic, the delayed diagnosis and treatment of cervical cancer have resulted in an increase in the number of patients and deaths. A previous study in Brazil showed that the proportion of women diagnosed with the International Federation of Gynecology and Obstetrics stage III–IV cervical cancer increased from 43.3% before the pandemic to 56.8% during the pandemic [34]. However, Gupta et al. [31] stated that the mortality rate (2.52%) associated with a 9-week delay in cervical cancer treatment was estimated to be 2.52%, which further increased to 3.8% due to a 6-month delay. According to various studies, in patients with cervical cancer, pelvic control decreases by 0.7–1% and the overall survival decreases by 0.6–0.8% each day for each additional day of interruption of standard 56-day radiotherapy treatment, which has a significant impact on the early stage of cervical cancer [35,36,37,38]. In the current COVID-19 pandemic, maximizing medical conditions to save and extend the lives of most patients is the highest priority [39, 40]. Gupta et al. [31] found that, compared with patients with advanced-stage cervical cancer, disease progression in patients with early-stage cervical cancer was more likely to be delayed by COVID-19. So when healthcare resources were stretched by the COVID-19 pandemic, many hospitals prioritized patients with diseases that could be cured or that could benefit from treatment. When medical resources are strained by a pandemic, they can be moderately tilted in patients who benefit more to reduce the adverse effects of a pandemic.

COVID-19 pandemic intensifying the anxiety and psychological stress of cervical cancer patients

The COVID-19 pandemic not only affects the treatment and prognosis of cervical cancer but also increases the psychological pressure and anxiety levels of patients with cervical cancer [41, 42]. During the COVID-19 pandemic, various preventive measures and a shortage of medical resources have made it more difficult for patients to seek medical care, causing anxiety among patients with various cancer types, including cervical cancer. Despite the heightened anxiety of patients caused by the pandemic, Ghosh et al. found that the majority of patients (68%) preferred to continue receiving chemotherapy; this finding suggests that patients may be more concerned about treating their cancer than the risk of contracting COVID-19 [43]; those receiving palliative chemotherapy are more concerned about their disease progression status than the risk of contracting COVID-19. This may be because they already know that their prognosis is poor and fear that their disease status will worsen during the COVID-19 pandemic. Hence, the medical staff can provide patients with more psychological comfort and support during treatment to help relieve their anxiety. Compared with the status when the COVID-19 pandemic first emerged in 2019, the people’s anxiety has gradually reduced owing to the enhanced understanding of COVID-19, the continuous update on COVID-19 treatment methods, and the development of COVID-19 vaccines. This finding suggests that doctors should focus on assessing anxiety levels and reducing anxiety in order to manage patients' mental health during the pandemic.

Increased risk of developing COVID-19 and serious events in patients with cervical cancer

Both malignancy and tumor treatment may lead to decreased physical capacity (performance status) and impaired immune status. Furthermore, patients have an increased need for medical care and hospitalization [44]. In the current pandemic, patients with cancer appear to be more likely to be diagnosed with COVID-19 and at a higher risk of experiencing severe events [45]. A previous study conducted by Chinese scholars showed that receiving tumor therapy in the last 14 days prior to infection was identified as a risk factor for developing serious events (hazard ratio: 4.07, 95% confidence interval: 1.08–15.3) [46]. The coronavirus receptor angiotensin-converting enzyme 2 (ACE2) and transmembrane serine protease 2 (TMPRSS2) play key roles in SARS-CoV-2-infected cells [47]. The expression levels of ACE2 and TMPRSS2 in different tumor cells may indicate the susceptibility of different tumors to COVID-19. ACE2 and TMPRSS2 are overexpressed in many cancers, including cervical squamous cell carcinoma and cervical adenocarcinoma [48, 49]. All of these factors may increase the risk of developing COVID-19 and serious events in patients with cervical cancer. With this in mind, determining the method of managing patients with cervical cancer during the COVID-19 pandemic is particularly important. Cervical cancer poses a considerable threat to the lives of patients, and delayed treatment may affect the effectiveness of cancer treatment. In this particular period of the COVID-19 pandemic, the recommendations for the management of cervical cancer should consider several aspects, including the staging of cervical cancer, choice of tumor treatment, local incidence of COVID-19, and local medical conditions.

Recommendations and lessons for the management of cervical cancer patients in developing countries during the pandemic

The incidence of cervical cancer is high in developing countries, which will face more challenges during the COVID-19 pandemic owing to the scarcity of healthcare resources in these countries [50]. Approximately 85% of cervical cancer cases occur in developing countries [51]. In these countries, the scarcity of medical resources were even more pronounced during the COVID-19 pandemic. In view of the management of cervical cancer in developing countries, with the maximum protection of the rights and interests of patients, Estevez-Diz et al. [50] provided some suggestions in Table 1.

Table 1 The summary of the recommendations for cervical cancer management during the COVID-19 pandemic
Full size table

Although cancer patients may have an increased risk of developing serious events related to COVID-19, tumor treatment in cancer patients cannot be substantially delayed to avoid endangering the tumor prognosis. Therefore, the doctors need to carefully consider the treatment management of different patients, and the management of each patient should be decided on a case-by-case basis; the doctors should determine the risks and benefits of each strategy.

Effect of the COVID-19 pandemic in the development of some HPV detection methods and the promotion of self-detection of HPV

The COVID-19 pandemic has affected the screening of HPV to a certain extent; however, in the current COVID-19 pandemic, some new virus detection methods have been used, such as bamboo shoots after a spring rain, which also greatly promoted the performance of HPV screening. These new detection methods, such as the TruScreen (TS01) test [52] (a portable instrument that uses optical and electrical signals to analyze cervical tissues with a built-in algorithm in real time), TR512-peptide-based virus detection [53] (which enables the TR512-peptide-based biorthogonal capture and enrichment of commercially available Texas red fluorophore-labeled nucleic acids on functionalized paper), and CRISPR-assisted DNA detection [54] (a novel dCas9-based DNA detection technique), can be used for the detection of HPV, has a low cost, high detection speed, and good specificity and sensitivity. The update and emergence of these testing methods will undoubtedly provide a great opportunity to eliminate cervical cancer. Therefore, an appropriate HPV testing method should be selected, and the goal of eliminating cervical cancer should be achieved.

Simultaneously, the COVID-19 pandemic has promoted the progress of HPV self-sampling. HPV self-sampling is similar to colon cancer screening at home via fecal tests. Self-sampling is a promising strategy; although it has not been approved for cervical cancer screening worldwide, self-collection of vaginal samples may contribute to better screening. The COVID-19 pandemic also promoted the application of this strategy [55]. A previous Nigerian study [56] has shown that delivering sealed, clean self-samplers to patients and self-collection greatly avoids exposure to COVID-19. Even after the termination of the current pandemic, a convenient method of sample self-collection would certainly promote HPV screening. Self-sampling can also be increasingly performed in countries with low cervical cancer screening rates or in areas with limited local medical resources (such as rural areas) [12]. Self-sampling for HPV testing can be demonstrated with simple graphics or animated videos to achieve the same accuracy as that of clinicians [57]. A study of 180,000 women in the Netherlands showed no difference in the sensitivity and specificity between self-sampling and physician-performed testing [58]. The promotion of self-sampling will also greatly promote cervical cancer screening, especially in areas where HPV screening cannot be completed due to economic backwardness and religious beliefs, and lay the groundwork for further achieving the WHO’s goal of eliminating cervical cancer.

Limitations of the study

This study summarizes the challenges and opportunities for cervical cancer during the COVID-19 pandemic, but is not a systematic study.

Conclusion

The COVID-19 pandemic has severely affected the screening, diagnosis, treatment and prevention of cervical cancer. The impact of cervical cancer will be especially significant in developing countries, where the majority of health resources are being allocated to combatting COVID-19 and are already limited. During the COVID-19 pandemic, the surgical treatment and chemotherapy of cervical cancer patients have been affected to varying degrees, and the radiotherapy and chemotherapy of many patients have been delayed, resulting in adverse outcomes such as disease progression, poor prognosis and increased mortality.

During the pandemic, patients with cervical cancer have also developed varying degrees of anxiety due to the delays in the treatment of their disease. Although much attention has been paid to managing the patient’s condition, providing care and understanding to the patient and improving their mental health should also be taken into consideration. Although some form of flow control strategy may be necessary to stop the spread of COVID-19, the healthcare systems should not only focus on curbing its spread but should also be reorganized to continue providing healthcare and necessary treatments [31]. In developing countries, the management of cervical cancer patients during the pandemic remains a challenge. Better management of patients with cervical cancer in this environment is an urgent matter that should be addressed. The management of cervical cancer varies from person to person, the clinical status of patients should be taken into account, and the pros and cons of the program should be weighed to maximize the protection of patients’ rights and interests. However, the COVID-19 environment brings not only challenges but also opportunities for cervical cancer management. Based on the detection methods used for COVID-19, some convenient and low-cost HPV detection strategies have been developed, and self-testing for HPV at home is promoted. The widespread application of this self-testing method will inevitably accelerate cervical cancer screening and contribute to the elimination of cervical cancer in the post-epidemic era.

Executive Summary

  1. 1.

    Several aspects of cervical cancer were greatly affected by the current pandemic.

  2. 2.

    The COVID pandemic has increased the tension on medical resources.

  3. 3.

    Healthcare-related inequalities have been further exacerbated by the pandemic.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

ACE2:

Angiotensin-converting enzyme 2

COVID-19:

Coronavirus disease 2019

HPV:

Human papillomavirus

SARS-CoV-2:

Severe acute respiratory syndrome coronavirus 2

TMPRSS2:

Transmembrane serine protease 2

WHO:

World Health Organization

References

  1. Niu Y, Luo L, Yang S, et al. Comparison of epidemiological characteristics and transmissibility of different strains of COVID-19 based on the incidence data of all local outbreaks in China as of March 1, 2022. Front Public Health. 2022;10:949594. https://doi.org/10.3389/fpubh.2022.949594.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Dinmohamed AG, Visser O, Verhoeven RHA, et al. Fewer cancer diagnoses during the COVID-19 epidemic in the Netherlands. Lancet Oncol. 2020;21(6):750–1. https://doi.org/10.1016/S1470-2045(20)30265-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Sud A, Torr B, Jones ME, et al. Effect of delays in the 2-week-wait cancer referral pathway during the COVID-19 pandemic on cancer survival in the UK: a modelling study. Lancet Oncol. 2020;21(8):1035–44. https://doi.org/10.1016/S1470-2045(20)30392-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hamilton W. Cancer diagnostic delay in the COVID-19 era: what happens next? Lancet Oncol. 2020;21(8):1000–2. https://doi.org/10.1016/S1470-2045(20)30391-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Jones D, Neal RD, Duffy SRG, et al. Impact of the COVID-19 pandemic on the symptomatic diagnosis of cancer: the view from primary care. Lancet Oncol. 2020;21(6):748–50. https://doi.org/10.1016/S1470-2045(20)30242-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Khanna D, Khargekar NC, Khanna AK. Implementation of early detection services for cancer in India during COVID-19 pandemic. Cancer Control. 2020;27(1):1073274820960471. https://doi.org/10.1177/1073274820960471.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Cancino RS, Su Z, Mesa R, et al. The impact of COVID-19 on cancer screening: challenges and opportunities. JMIR Cancer. 2020;6(2):e21697. https://doi.org/10.2196/21697.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Meggetto O, Jembere N, Gao J, et al. The impact of the COVID-19 pandemic on the Ontario Cervical Screening Program, colposcopy and treatment services in Ontario, Canada: a population-based study. BJOG. 2021;128(9):1503–10. https://doi.org/10.1111/1471-0528.16741.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Feletto E, Grogan P, Nickson C, et al. How has COVID-19 impacted cancer screening? Adaptation of services and the future outlook in Australia. Public Health Res Pract. 2020. https://doi.org/10.17061/phrp3042026.

    Article  PubMed  Google Scholar 

  10. Poljak M, Cuschieri K, Waheed DE, et al. Impact of the COVID-19 pandemic on human papillomavirus-based testing services to support cervical cancer screening. Acta Dermatovenerol Alp Pannonica Adriat. 2021;30(1):21–6.

    PubMed  Google Scholar 

  11. Shen CT, Hsieh HM, Chang YL, et al. Different impacts of cancer types on cancer screening during COVID-19 pandemic in Taiwan. J Formos Med Assoc. 2022;121(10):1993–2000. https://doi.org/10.1016/j.jfma.2022.02.006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Poniewierza P, Panek G. Cervical cancer prevention in the era of the COVID-19 pandemic. Medicina (Kaunas). 2022. https://doi.org/10.3390/medicina58060732.

    Article  PubMed  Google Scholar 

  13. Castanon A, Rebolj M, Pesola F, et al. COVID-19 disruption to cervical cancer screening in England. J Med Screen. 2022;29(3):203–8. https://doi.org/10.1177/09691413221090892.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Sasidharanpillai S, Ravishankar N. The short-term impact Of COVID-19 pandemic on cervical cancer screening: a systematic review and meta-analysis. Asian Pac J Cancer Prev. 2022;23(5):1497–504. https://doi.org/10.31557/APJCP.2022.23.5.1497.

    Article  PubMed  Google Scholar 

  15. Smith MA, Burger EA, Castanon A, et al. Impact of disruptions and recovery for established cervical screening programs across a range of high-income country program designs, using COVID-19 as an example: a modelled analysis. Prev Med. 2021;151:106623. https://doi.org/10.1016/j.ypmed.2021.106623.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Wentzensen N, Clarke MA, Perkins RB. Impact of COVID-19 on cervical cancer screening: challenges and opportunities to improving resilience and reduce disparities. Prev Med. 2021;151:106596. https://doi.org/10.1016/j.ypmed.2021.106596.

    Article  PubMed  PubMed Central  Google Scholar 

  17. DeGroff A, Miller J, Sharma K, et al. COVID-19 impact on screening test volume through the National Breast and Cervical Cancer early detection program, January–June 2020, in the United States. Prev Med. 2021;151:106559. https://doi.org/10.1016/j.ypmed.2021.106559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Shamseddine AA, Burman B, Lee NY, et al. Tumor immunity and immunotherapy for HPV-related cancers. Cancer Discov. 2021;11(8):1896–912. https://doi.org/10.1158/2159-8290.cd-20-1760.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kamolratanakul S, Pitisuttithum P. Human papillomavirus vaccine efficacy and effectiveness against cancer. Vaccines (Basel). 2021. https://doi.org/10.3390/vaccines9121413.

    Article  PubMed  Google Scholar 

  20. Wang R, Pan W, Jin L, et al. Human papillomavirus vaccine against cervical cancer: opportunity and challenge. Cancer Lett. 2020;471:88–102. https://doi.org/10.1016/j.canlet.2019.11.039.

    Article  CAS  PubMed  Google Scholar 

  21. Meites E, Szilagyi PG, Chesson HW, et al. Human papillomavirus vaccination for adults: updated recommendations of the advisory committee on immunization practices. MMWR Morb Mortal Wkly Rep. 2019;68(32):698–702. https://doi.org/10.15585/mmwr.mm6832a3.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Saxena K, Marden JR, Carias C, et al. Impact of the COVID-19 pandemic on adolescent vaccinations: projected time to reverse deficits in routine adolescent vaccination in the United States. Curr Med Res Opin. 2021;37(12):2077–87. https://doi.org/10.1080/03007995.2021.1981842.

    Article  CAS  PubMed  Google Scholar 

  23. Olagoke AA, Carnahan LR, Olagoke O, et al. Shared determinants for human papillomavirus and COVID-19 vaccination intention: an opportunity for resource consolidation. Am J Health Promot. 2022;36(3):506–9. https://doi.org/10.1177/08901171211053933.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Sycinska-Dziarnowska M, Paradowska-Stankiewicz I, Woźniak K. The global interest in vaccines and its prediction and perspectives in the era of COVID-19. Real-time surveillance using Google trends. Int J Environ Res Public Health. 2021. https://doi.org/10.3390/ijerph18157841.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Kregting LM, Kaljouw S, de Jonge L, et al. Effects of cancer screening restart strategies after COVID-19 disruption. Br J Cancer. 2021;124(9):1516–23. https://doi.org/10.1038/s41416-021-01261-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Koczkodaj P, Kamiński M, Ciuba A, et al. Cancer screening coverage in Poland—from bad to better to the worst during the SARS-CoV-2 pandemic. Arch Med Sci. 2021;17(4):1132–3. https://doi.org/10.5114/aoms/134239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Le Bihan BC, Simonnet J-A, Rocchi M, et al. Monitoring the impact of COVID-19 in France on cancer care: a differentiated impact. Sci Rep. 2022;12(1):4207. https://doi.org/10.1038/s41598-022-07984-w.

    Article  CAS  Google Scholar 

  28. Ginsburg O, Basu P, Kapambwe S, et al. Eliminating cervical cancer in the COVID-19 era. Nature Cancer. 2021;2(2):133–4. https://doi.org/10.1038/s43018-021-00178-9.

    Article  CAS  PubMed  Google Scholar 

  29. Kepka D, Christini K, McGough E, et al. Successful multi-level HPV vaccination intervention at a rural healthcare center in the era of COVID-19. Front Digit Health. 2021;3:719138. https://doi.org/10.3389/fdgth.2021.719138.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Jouen T, Gauthier T, Azais H, et al. The impact of the COVID-19 coronavirus pandemic on the surgical management of gynecological cancers: Analysis of the multicenter database of the French SCGP and the FRANCOGYN group. J Gynecol Obstet Hum Reprod. 2021;50(8):102133. https://doi.org/10.1016/j.jogoh.2021.102133.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Gupta N, Chauhan AS, Prinja S, et al. Impact of COVID-19 on outcomes for patients with cervical cancer in India. JCO Glob Oncol. 2021;7:716–25. https://doi.org/10.1200/go.20.00654.

    Article  PubMed  Google Scholar 

  32. Pramesh CS, Badwe RA. Cancer management in India during Covid-19. N Engl J Med. 2020;382(20):e61. https://doi.org/10.1056/NEJMc2011595.

    Article  CAS  PubMed  Google Scholar 

  33. The LO. COVID-19: global consequences for oncology. Lancet Oncol. 2020;21(4):467. https://doi.org/10.1016/s1470-2045(20)30175-3.

    Article  CAS  Google Scholar 

  34. Bonadio RC, Messias AP, Moreira OA, et al. Impact of the COVID-19 pandemic on breast and cervical cancer stage at diagnosis in Brazil. Ecancermedicalscience. 2021;15:1299. https://doi.org/10.3332/ecancer.2021.1299.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Girinsky T, Rey A, Roche B, et al. Overall treatment time in advanced cervical carcinomas: a critical parameter in treatment outcome. Int J Radiat Oncol Biol Phys. 1993;27(5):1051–6. https://doi.org/10.1016/0360-3016(93)90522-w.

    Article  CAS  PubMed  Google Scholar 

  36. Perez CA, Grigsby PW, Castro-Vita H, et al. Carcinoma of the uterine cervix. I. Impact of prolongation of overall treatment time and timing of brachytherapy on outcome of radiation therapy. Int J Radiat Oncol Biol Phys. 1995;32(5):1275–88. https://doi.org/10.1016/0360-3016(95)00220-s.

    Article  CAS  PubMed  Google Scholar 

  37. Petereit DG, Sarkaria JN, Chappell R, et al. The adverse effect of treatment prolongation in cervical carcinoma. Int J Radiat Oncol Biol Phys. 1995;32(5):1301–7. https://doi.org/10.1016/0360-3016(94)00635-x.

    Article  CAS  PubMed  Google Scholar 

  38. Lin SM, Ku HY, Chang TC, et al. The prognostic impact of overall treatment time on disease outcome in uterine cervical cancer patients treated primarily with concomitant chemoradiotherapy: a nationwide Taiwanese cohort study. Oncotarget. 2017;8(49):85203–13. https://doi.org/10.18632/oncotarget.19617.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Prinja S, Pandav CS. Economics of COVID-19: challenges and the way forward for health policy during and after the pandemic. Indian J Public Health. 2020;64(Supplement):S231-s233. https://doi.org/10.4103/ijph.IJPH_524_20.

    Article  PubMed  Google Scholar 

  40. Emanuel EJ, Persad G, Upshur R, et al. Fair allocation of scarce medical resources in the time of covid-19. N Engl J Med. 2020;382(21):2049–55. https://doi.org/10.1056/NEJMsb2005114.

    Article  PubMed  Google Scholar 

  41. Li CC, Feng TH. Talk about psychological distress and support in women with gynecological cancer: NOT just the disease. Hu Li Za Zhi. 2022;69(4):20–6. https://doi.org/10.6224/jn.202208_69(4).04.

    Article  PubMed  Google Scholar 

  42. Min Y, Liu Z, Huang R, et al. Survival outcomes following treatment delays among patients with early-stage female cancers: a nationwide study. J Transl Med. 2022;20(1):560. https://doi.org/10.1186/s12967-022-03719-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ghosh J, Ganguly S, Mondal D, et al. Perspective of oncology patients during COVID-19 pandemic: a prospective observational study from India. JCO Glob Oncol. 2020;6:844–51. https://doi.org/10.1200/go.20.00172.

    Article  PubMed  Google Scholar 

  44. Al-Shamsi HO, Alhazzani W, Alhuraiji A, et al. A practical approach to the management of cancer patients during the novel coronavirus disease 2019 (COVID-19) pandemic: an international collaborative group. Oncologist. 2020;25(6):e936–45. https://doi.org/10.1634/theoncologist.2020-0213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Sidaway P. COVID-19 and cancer: what we know so far. Nat Rev Clin Oncol. 2020;17(6):336. https://doi.org/10.1038/s41571-020-0366-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Zhang L, Zhu F, Xie L, et al. Clinical characteristics of COVID-19-infected cancer patients: a retrospective case study in three hospitals within Wuhan, China. Ann Oncol. 2020;31(7):894–901. https://doi.org/10.1016/j.annonc.2020.03.296.

    Article  CAS  PubMed  Google Scholar 

  47. Hoffmann M, Kleine-Weber H, Schroeder S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181(2):271-280.e278. https://doi.org/10.1016/j.cell.2020.02.052.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Li H, Xie L, Chen L, et al. Genomic, epigenomic, and immune subtype analysis of CTSL/B and SARS-CoV-2 receptor ACE2 in pan-cancer. Aging (Albany NY). 2020;12(22):22370–89. https://doi.org/10.18632/aging.104147.

    Article  CAS  PubMed  Google Scholar 

  49. Katopodis P, Anikin V, Randeva HS, et al. Pan-cancer analysis of transmembrane protease serine 2 and cathepsin L that mediate cellular SARS-CoV-2 infection leading to COVID-19. Int J Oncol. 2020;57(2):533–9. https://doi.org/10.3892/ijo.2020.5071.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Del Pilar E-D, Bonadio RC, Miranda VC, et al. Management of cervical cancer patients during the COVID-19 pandemic: a challenge for developing countries. Ecancermedicalscience. 2020;14:1060. https://doi.org/10.3332/ecancer.2020.1060.

    Article  Google Scholar 

  51. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. https://doi.org/10.3322/caac.21492.

    Article  PubMed  Google Scholar 

  52. Wang Z, Kang Y, Yu F, et al. TruScreen detection of cervical tissues for high-risk human papillomavirus-infected women during the COVID-19 pandemic. Future Oncol. 2021;17(10):1197–207. https://doi.org/10.2217/fon-2020-0928.

    Article  CAS  PubMed  Google Scholar 

  53. Zhu M, Huangfu C, Wan W, et al. A Novel virus detection strategy enabled by TR512-peptide-based bioorthogonal capture and enrichment of preamplified nucleic acid. Anal Chem. 2022;94(14):5591–8. https://doi.org/10.1021/acs.analchem.1c05315.

    Article  CAS  PubMed  Google Scholar 

  54. Xu X, Luo T, Gao J, et al. CRISPR-Assisted DNA detection: a novel dCas9-Based DNA detection technique. CRISPR J. 2020;3(6):487–502. https://doi.org/10.1089/crispr.2020.0041.

    Article  CAS  PubMed  Google Scholar 

  55. Ajenifuja KO, Belinson J, Goldstein A, et al. Designing low-cost, accurate cervical screening strategies that take into account COVID-19: a role for self-sampled HPV typing2. Infect Agent Cancer. 2020;15:61. https://doi.org/10.1186/s13027-020-00325-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Desai KT, Ajenifuja KO, Banjo A, et al. Design and feasibility of a novel program of cervical screening in Nigeria: self-sampled HPV testing paired with visual triage. Infect Agent Cancer. 2020;15:60. https://doi.org/10.1186/s13027-020-00324-5.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Lam JU, Rebolj M, Møller Ejegod D, et al. Human papillomavirus self-sampling for screening nonattenders: opt-in pilot implementation with electronic communication platforms. Int J Cancer. 2017;140(10):2212–9. https://doi.org/10.1002/ijc.30647.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Serrano B, Ibáñez R, Robles C, et al. Worldwide use of HPV self-sampling for cervical cancer screening. Prev Med. 2022;154:106900. https://doi.org/10.1016/j.ypmed.2021.106900.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Editage (www.editage.cn) for English language editing.

Funding

This study was supported by the "Clinical Medicine +X" research project QDFY + X202101025 of the Affiliated Hospital of Qingdao University and the 2021-WJZD196 Qingdao Medical and Health Research Project.

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Authors and Affiliations

  1. Department of Obstetrics & Gynecology, The Affiliated Hospital of Qingdao University, Jiangsu Road No. 16, Shinan District, Qingdao, 266000, China

    Shixiang Dong & Yankui Wang

  2. Department of Reproductive Medicine, The Affiliated Hospital of Qingdao University, 59 Haier Road, Qingdao, 266000, China

    Yu Ding

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  1. Shixiang Dong
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  2. Yankui Wang
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SD: Writing—Original Draft, YW: Supervision, YD: Supervision and Funding Acquisition. All authors read and approved the final manuscript.

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Correspondence to Yankui Wang or Yu Ding.

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Dong, S., Wang, Y. & Ding, Y. Opportunities and challenges encountered in managing cervical cancer during the coronavirus disease 2019 pandemic. Infect Agents Cancer 19, 41 (2024). https://doi.org/10.1186/s13027-024-00594-3

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Keywords

Infectious Agents and Cancer

ISSN: 1750-9378

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