Pan-Canadian survey on the impact of the COVID-19 pandemic on cervical cancer screening and management: cross-sectional survey of healthcare professionals

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    This study explored practitioners' assessments of the impact of the pandemic on cervical cancer screening and follow-up. This is a very important topic that could continue to have implications for how this screening process is delivered now, after the pandemic. The authors need to more fully describe their methodology and temper conclusions to fit within those limitations.

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Abstract

The coronavirus disease 2019 (COVID-19) pandemic has caused disruptions to cancer care by delaying diagnoses and treatment, presenting challenges and uncertainties for both patients and physicians. We conducted a nationwide online survey to investigate the effects of the pandemic and capture modifications, prompted by pandemic-related control measures, on cervical cancer screening-related activities from mid-March to mid-August 2020, across Canada.

Methods:

The survey consisted of 61 questions related to the continuum of care in cervical cancer screening and treatment: appointment scheduling, tests, colposcopy, follow-up, treatment of pre-cancerous lesions/cancer, and telemedicine. We piloted the survey with 21 Canadian experts in cervical cancer prevention and care. We partnered with the Society of Canadian Colposcopists, Society of Gynecologic Oncology of Canada, Canadian Association of Pathologists, and Society of Obstetricians and Gynecologists of Canada, which distributed the survey to their members via email. We reached out to family physicians and nurse practitioners via MDBriefCase. The survey was also posted on McGill Channels (Department of Family Medicine News and Events) and social media platforms. The data were analyzed descriptively.

Results:

Unique responses were collected from 510 participants (November 16, 2020, to February 28, 2021), representing 418 fully and 92 partially completed surveys. Responses were from Ontario (41.0%), British Columbia (21.0%), and Alberta (12.8%), and mostly comprised family physicians/general practitioners (43.7%), and gynecologist/obstetrician professionals (21.6%). Cancelled screening appointments were mainly reported by family physicians/general practitioners (28.3%), followed by gynecologist/obstetrician professionals (19.8%), and primarily occurred in private clinics (30.5%). Decreases in the number of screening Pap tests and colposcopy procedures were consistently observed across Canadian provinces. About 90% reported that their practice/institution adopted telemedicine to communicate with patients.

Conclusions:

The area most severely impacted by the pandemic was appointment scheduling, with an important level of cancellations reported. Survey results may inform resumptions of various fronts in cervical cancer screening and management.

Funding:

The present work was supported by the Canadian Institutes of Health Research (operating grant COVID-19 May 2020 Rapid Research Funding Opportunity VR5-172666 Rapid Research competition and foundation grant 143347 to Eduardo L Franco). Eliya Farah and Rami Ali each received an MSc stipend from the Department of Oncology, McGill University.

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  1. Author Response

    Reviewer #1 (Public Review):

    During the height of the Covid19-pandemic, there was great and widely spread concern about the lowered protection the screening programs within the cancer area could offer. Not only were programs halted for some periods because of a lack of staff or concern about the spreading of SARS CoV2. When screening activities were upheld, participation decreased, and follow-up of positive test results was delayed. Mariam El-Zein and coworkers have addressed this concern in the context of cervical screening in Canada, one of the rather few countries in the world with well organized, population-based, although regionalized, cervical screening program.

    Comment 1: Despite the existence of screening registries, they choose to do this in form of a survey on the internet, to different professional groups within the chain of care in cervical screening and colposcopy. The reason for taking this "soft data" approach is somewhat diffuse.

    We are happy to provide a counterargument to the reviewer’s concern about the “soft data” approach. Our unit – McGill’s Division of Cancer Epidemiology – is a major stakeholder in policymaking and cervical screening guideline development in Canada. It is one of the components in a McGill Task Force on COVID-19 and Cancer that has been widely engaged in assessing the pandemic’s impact on the entire spectrum of cancer control and care (examples: PMID: 33669102, PMID: 34843106). Canada is a country of continental size, and during the pandemic even travel between provinces was interrupted. It is only via a web-based survey that one could have captured the required information. We took advantage of our unit’s credibility and stature to secure a substantial response to the survey, which elicited a high level of detail.

    The survey questionnaire instrument was thoughtfully developed with input from Canadian experts who are active in the field of cervical cancer prevention and involved in clinical care to comprehensively formulate informative questions (and practical, reasonable responses) underpinning each of the themes covered. Of note, some of these coinvestigators, having executive roles in relevant clinical professional bodies, advised our team on the logistics of circulating the survey to members. The administration of the survey was coordinated with the pertinent societies. Our aim was to provide an overall portrait across Canada of the extent of the harms to cervical cancer screening and treatment processes at the beginning of the COVID-19 pandemic (specifically a snapshot from mid-March to mid-August 2020), as perceived by professional groups in multiple health disciplines.

    Indeed, as the reviewer mentioned, there are fully (i.e., for Saskatchewan) and partially (i.e., for British Columbia, Alberta, Manitoba, Ontario) organized cervical cancer screening programs in Canada in addition to opportunistic programs (i.e., for North West Territories, Yukon, Nunavut, Quebec). The Canadian Partnership Against Cancer also collects information on cervical cancer screening programs and/or strategies across Canada. Using data from these different sources enables a quantitative assessment of the impact of the pandemic on cervical cancer screening, but this was not the research methodology used; the survey approach was our research strategy as we attempted to collect responses from all provinces and territories, regardless of the different screening programs and modalities implemented across the country, and including regions that do not have an official screening program.

    Since the effects of the COVID-19 pandemic will stay with us for years to come, our research team is also examining – using a “hard data” approach via administrative healthcare datasets – the long-term effects that will accrue on cervical cancer morbidity and mortality from the interruptions and delays in screening processes and other activities in the process of care. A discussion of this is, however, beyond the scope and objectives of our manuscript.

    No modifications were made in the manuscript to address this comment.

    Comment 2: The authors claim they want to "capture modifications". However, the suggestions that come from this study are limited and are submitted for publication 2 years after the survey when the height of the pandemic has passed long since, and its burden on the screening program has largely disappeared. The value of the study had been larger if either the conclusions had been communicated almost directly, or if the survey had been done later, to sum up the total effect of the pandemic on the Canadian cervical screening program.

    We appreciate this comment. As part of our commitment to transparency, we now plainly acknowledge that considerable time (1.5 years) has elapsed between the time the survey data were available (March 2021) and manuscript submission (September 2022) for publication in the special issue, curated by eLife, on the impact of the COVID-19 pandemic on cancer prevention, control, care and survivorship. However, we also argue that this lag time is reasonable given the undertaking of data management, analysis, and reporting of a large amount of data, including the synthesis of replies to open-ended questions. We also took this opportunity to expose two graduate students to the research process.

    Changes made: Page 15, Lines 437-440.

    In terms of assessing the total effect of the pandemic on the Canadian cervical screening program, this work is in progress, but not within the current manuscript. The PubMed references mentioned above show examples of directions we are taking. Also, as mentioned in our response 1 to comment 1, we will use data from administrative healthcare datasets (medical and drug claims, hospitalization data, death registry data) and hospital cancer registries (clinical characteristics such as cancer stage, grade, and biomarkers) on cancer patients diagnosed in Quebec between 2010 and 2026. Using these datasets, we intend to compare the pre- and post-pandemic eras in order to analyze changes in patterns of cancer care, cancer prognosis, and survival, including shifts at stage at diagnosis.

    Comment 3: Another major problem with this study is the coverage. The results of persistent activities to get a large uptake is somewhat depressing although this is not expressed by the authors. 510 professionals filled out the survey partially or in total. 10 professions were targeted. The authors make no attempt to assess the coverage or the validity of the sample. They state the method used does not make that possible. But the number of family practicians, colposcopists, cytotechnicians, etc. involved in the program should roughly be known and the proportion of those who answered the survey could have been calculated. My guess is that it is far below 10%.

    There were no extensive additional efforts to increase participation rate, apart from follow-up reminder emails to complete the survey, which is standard practice followed by the societies that administered the survey to their constituents. We respectfully disagree with the reviewer concerning coverage being a major limitation, particularly in view of the difficulty in general to secure a high response rate in a survey such as ours, at a time like the middle of the pandemic. Although it appears to be a seemingly easy to compute classic non-response rate, information on the “population of interest” (i.e., number of professionals approached in addition to the advertisement of the survey on social media platform”) is not available to estimate the extent of non-response. Even if the response rate is below 10% as suggested by the Reviewer, our survey and findings should be considered on their merits; the target population was involved in the survey design to ensure the validity of coverage of the questions along the continuum of care in cervical cancer screening and treatment. In addition, we followed the Checklist for Reporting Results of Internet E-surveys to inform the design, conduct, and reporting of our survey research.

    Changes made: Page 14, Lines 421-425.

    Comment 4: The national distribution seems shewed despite the authors boosting its pan-Canadian character. I am just faintly familiar with the Canadian regions, but, as an example, only 2 replies from Quebec must question the national validity of this survey.

    We apologize for this typo error in Table 1; many cells were accidently shifted down (the last couple of provinces had the wrong numbers). There were actually 21 survey respondents from the province of Quebec. This has now been corrected.

    Changes made: Page 19.

    Comment 5: The result section is dominated by quantitative data from the responses to the 61 questions. All questions and their answers are tabulated. As there is no way to assess the selection bias of the answers these quantitative results have no real value from an epidemiological standpoint.

    Indeed, we opted to provide the reader with descriptive results on all the questions and sub-questions that were asked, with explicit annotation to each question number and clear reference to the formulated question by appending the full survey instrument to the manuscript. We designed the survey as a descriptive and not an analytical study, contrary to traditional epidemiology studies that investigate a specific exposure-outcome relationship.

    Changes made: Page 12, Lines 366-368.

    In the spirit of other papers in the special issue on COVID-19 and cancer, curated by eLife, we measured the impact of the pandemic on the process of care like many other eLife articles did. The eLife collection is a snapshot of a period when not only was cancer control disrupted, but the ability to conduct valid research was also severely curtailed. The reviewer will likely agree that our paper is not the only one to suffer from these methodological shortcomings. Yet, taken together, the gestalt value of the eLife collection will inform epidemiologic modellers for the next long while on how this period affected cancer control. We are happy to contribute with this paper a few more pieces of the puzzle, adding to that which eLife published for many other jurisdictions.

    Comment 6: The replies to the open-ended questions are summarized in a table and in the text. The main conclusion of the content analysis of the answers to the direct questions, and one of the main conclusions of the study, is that the majority favors HPV self-sampling in light of the pandemic. However, this not-surprising view is taken by only 80 responders while almost as many (n=60) had no knowledge about HPV self-sampling.

    Another aim of our survey was to identify the windows of opportunity that were created by the pandemic and pinpoint positive aspects that could enable the transformation of cervical cancer screening (i.e., HPV primary based screening and HPV self-sampling). We found that 33% of respondents were of the opinion that the pandemic context could facilitate the implementation of self-sampling and that 50.1% were in favor of the implementation of this new screening practice (described in Results Theme 1: Screening Practice and Stable 5).

    Changes made: Page 4, Lines 93-97.

    The reviewer is correct that in the open-ended sub-question of Question 23 “Are you in favor of the implementation of HPV self-sampling as an alternative screening method in your clinical practice?”, 60 respondents justified their answer to the nominal question by their lack of familiarity with HPV self-sampling, compared to 80 who shared positive comments. However, we would like to draw the reviewer’s attention to the responses to the nominal part of the question in Stable 5. Of those who answered “Maybe”, 47.1% said that they were not familiar enough to express a favorable or unfavorable opinion. We would also like to draw the reviewer’s attention to the results of our cross-tabulation of profession and the question of relevance (described in Results Theme 1: Screening Practice). The lack of familiarity with novel screening practices such as self-sampling can be explained by the fact that most (75.0%) of those who expressed these views were primary healthcare professionals, and not secondary and tertiary specialists.

    Changes made: Page 12, Lines 344-346

    Comment 7: The authors conclude that their study identified the need for recommendations and strategies and building resilience in the screening system. No one would dispute the need, but the additional weight this study adds, unfortunately, is low, from a scientific standpoint.

    Although no one would dispute the need as the reviewer is suggesting, but as epidemiologists we needed to collect this empirical evidence. We urge the reviewer to consider that this article is to contribute to a more complete picture of the collective process of discovery of the impact of the pandemic initiated by eLife’s special issue.

    No modifications were made in the manuscript to address this comment.

    Comment 8: The conclusion I draw from this study is that the authors have done a good job in identifying some possible areas within the Canadian screening programs where the SARS-Cov2 pandemic had negative effects and received some support for that in a survey. Furthermore, they listed a few actions that could be taken to alleviate the vulnerability of the program in a future similar situation, and received limited support for that. No more, no less.

    We thank the Reviewer for the positive feedback provided in the first part of the comment. As for the rest, we believe we have addressed above the reviewer’s concerns.

    Reviewer #2 (Public Review):

    The study aimed to provide information on the extent to which the COVID-19 pandemic impacted cervical cancer (CC) screening and treatment in 3 Canadian provinces. The survey methodology is appropriate, and the results provide detailed descriptive statistics by province and type of practice. The results support the authors' conclusions. This evidence together with data gathered from other national surveys may provide baseline data on the impact of the pandemic on CC outcomes such as late-stage diagnoses and CC treatment outcomes due to these delays.

    We are flattered by the Reviewer’s overall assessment of our manuscript.

    Comment: This study relies mostly on descriptive statistics and open-ended questions that provide details about what CC screening and treatment procedures were delayed. It is unclear how the reader would use the results to affect current or future practice.

    As mentioned in our reply above to a similar comment raised by reviewer 1, our overarching aim was to portray in a purely descriptive manner the negative and positive impacts of the COVID-19 pandemic on cervical cancer screening-related activities, as perceived by healthcare professionals. Please refer to arguments above.

    Changes made: Page 12, Lines 366-368; Page 15, Lines 437-440.

  2. eLife assessment

    This study explored practitioners' assessments of the impact of the pandemic on cervical cancer screening and follow-up. This is a very important topic that could continue to have implications for how this screening process is delivered now, after the pandemic. The authors need to more fully describe their methodology and temper conclusions to fit within those limitations.

  3. Reviewer #1 (Public Review):

    During the height of the Covid19-pandemic, there was great and widely spread concern about the lowered protection the screening programs within the cancer area could offer. Not only were programs halted for some periods because of a lack of staff or concern about the spreading of SARS CoV2. When screening activities were upheld, participation decreased, and follow-up of positive test results was delayed. Mariam El-Zein and coworkers have addressed this concern in the context of cervical screening in Canada, one of the rather few countries in the world with well organized, population-based, although regionalized, cervical screening program.

    Despite the existence of screening registries, they choose to do this in form of a survey on the internet, to different professional groups within the chain of care in cervical screening and colposcopy. The reason for taking this "soft data" approach is somewhat diffuse. The authors claim they want to "capture modifications". However, the suggestions that come from this study are limited and are submitted for publication 2 years after the survey when the height of the pandemic has passed long since, and its burden on the screening program has largely disappeared. The value of the study had been larger if either the conclusions had been communicated almost directly, or if the survey had been done later, to sum up the total effect of the pandemic on the Canadian cervical screening program.

    Another major problem with this study is the coverage. The results of persistent activities to get a large uptake is somewhat depressing although this is not expressed by the authors. 510 professionals filled out the survey partially or in total. 10 professions were targeted. The authors make no attempt to assess the coverage or the validity of the sample. They state the method used does not make that possible. But the number of family practicians, colposcopists, cytotechnicians, etc. involved in the program should roughly be known and the proportion of those who answered the survey could have been calculated. My guess is that it is far below 10%. Also, the national distribution seems shewed despite the authors boosting its pan-Canadian character. I am just faintly familiar with the Canadian regions, but, as an example, only 2 replies from Quebec must question the national validity of this survey.

    The result section is dominated by quantitative data from the responses to the 61 questions. All questions and their answers are tabulated. As there is no way to assess the selection bias of the answers these quantitative results have no real value from an epidemiological standpoint. The replies to the open-ended questions are summarized in a table and in the text. The main conclusion of the content analysis of the answers to the direct questions, and one of the main conclusions of the study, is that the majority favors HPV self-sampling in light of the pandemic. However, this not-surprising view is taken by only 80 responders while almost as many (n=60) had no knowledge about HPV self-sampling.

    The authors conclude that their study identified the need for recommendations and strategies and building resilience in the screening system. No one would dispute the need, but the additional weight this study adds, unfortunately, is low, from a scientific standpoint.

    The conclusion I draw from this study is that the authors have done a good job in identifying some possible areas within the Canadian screening programs where the SARS-Cov2 pandemic had negative effects and received some support for that in a survey. Furthermore, they listed a few actions that could be taken to alleviate the vulnerability of the program in a future similar situation, and received limited support for that. No more, no less.

  4. Reviewer #2 (Public Review):

    The study aimed to provide information on the extent to which the COVID-19 pandemic impacted cervical cancer (CC) screening and treatment in 3 Canadian provinces. The survey methodology is appropriate, and the results provide detailed descriptive statistics by province and type of practice. The results support the authors' conclusions. This evidence together with data gathered from other national surveys may provide baseline data on the impact of the pandemic on CC outcomes such as late-stage diagnoses and CC treatment outcomes due to these delays.