Work

Author response: Examining the perceived impact of the COVID-19 pandemic on cervical cancer screening practices among clinicians practicing in Federally Qualified Health Centers: A mixed methods study

Year: 2023

Type: peer-review

Abstract: Full text Figures and data Side by side Abstract Editor's evaluation Introduction Methods Results Discussion Data availability References Decision letter Author response Article and author information Metrics Abstract Background: The COVID-19 pandemic led to reductions in cervical cancer screening and colposcopy. Therefore, in this mixed methods study we explored perceived pandemic-related practice changes to cervical cancer screenings in federally qualified health centers (FQHCs). Methods: Between October 2021 and June 2022, we conducted a national web survey of clinicians (physicians and advanced practice providers) who performed cervical cancer screening in FQHCs in the United States during the post-acute phase of the COVID-19 pandemic, along with a sub-set of qualitative interviews via video conference, to examine perceived changes in cervical cancer screening practices during the pandemic. Results: A total of 148 clinicians completed surveys; a subset (n=13) completed qualitative interviews. Most (86%) reported reduced cervical cancer screening early in the pandemic, and 28% reported continued reduction in services at the time of survey completion (October 2021- July 2022). Nearly half (45%) reported staff shortages impacting their ability to screen or track patients. Compared to clinicians in Obstetrics/Gynecology/Women’s health, those in family medicine and other specialties more often reported reduced screening compared to pre-pandemic. Most (92%) felt that screening using HPV self-sampling would be very or somewhat helpful to address screening backlogs. Qualitative interviews highlighted the impacts of staff shortages and strategies for improvement. Conclusions: Findings highlight that in late 2021 and early 2022, many clinicians in FQHCs reported reduced cervical cancer screening and of pandemic-related staffing shortages impacting screening and follow-up. If not addressed, reduced screenings among underserved populations could worsen cervical cancer disparities in the future. Funding: This study was funded by the American Cancer Society, who had no role in the study’s design, conduct, or reporting. Editor's evaluation This US study presents findings from an online survey and in-person interviews of healthcare providers in areas associated with cervical screening provision during the post-acute phase of the pandemic. The findings are valuable as they provide insights into a range of areas, from healthcare characteristics to screening barriers and HPV self-sampling. The evidence supporting the claims of the authors is solid. The work will be of interest to public health scientists and a cancer prevention and control audience. https://doi.org/10.7554/eLife.86358.sa0 Decision letter Reviews on Sciety eLife's review process Introduction Cervical cancer prevention via screening and treatment of pre-invasive disease has dramatically reduced cervical cancer incidence and mortality rates (Sawaya and Huchko, 2017). However, lack of access to screening and treatment services results in geographic, racial/ethnic, and socioeconomic disparities in cervical cancer incidence and mortality (Buskwofie et al., 2020; Vu et al., 2018; Chen et al., 2012; Akers et al., 2007). A recent study of cervical cancer patients showed that over half were either never screened or were overdue for screening (Benard et al., 2021). Lack of screening remains the most common reason why individuals develop cervical cancer in the United States (US) and worldwide. In the US, cervical cancer screening is considered a critical element of preventive healthcare, and the addition of Human Papillomavirus (HPV) testing, along with Pap testing, can improve prevention programs by allowing longer screening intervals for patients testing negative, while providing more precise risk estimates to allow evidence-based management of patients with abnormal screening results (Schiffman et al., 2011; Leinonen et al., 2009; Mayrand et al., 2007). Since the COVID-19 pandemic began in the US in 2020, however, cancer screenings decreased for many cancer types (Chen et al., 2021; Poljak et al., 2021; Amram et al., 2022; Smith and Perkins, 2022), with cervical cancer screening decreasing more than others (Miller et al., 2021; Mayo et al., 2021; Fedewa et al., 2022). Early in the pandemic, patient fear of contracting COVID-19 and reduction in non-urgent medical services impacted the ability to perform cervical cancer screening and colposcopy (Massad, 2022). Federally qualified health centers (FQHCs) in the US are government funded health centers or clinics that provide care to medically underserved populations. Maintaining cancer screening in these and other safety net facilities is critical as they serve patients at the highest risk for cervical cancer: publicly insured/uninsured, immigrant, and historically marginalized populations (Adams et al., 2020; Fisher-Borne et al., 2021). A survey of 22 federally qualified health centers (FQHCs) that conducted cervical cancer screenings in 2020 found that 90% reported cancelling cervical cancer screenings during the height of the pandemic (Fisher-Borne et al., 2021). While 86% reported rescheduling cancer screenings for future visits, the success of this strategy to maintain screening rates was not measured. FQHCs reported strategies such as switching to telehealth visits and implementing in-office structural changes, new waiting room protocols, and new referral processes to address pandemic restrictions (Fisher-Borne et al., 2021). Following widespread vaccination and the resumption of in person services, cancer screening rates have begun to rebound (Chen et al., 2021; McBain et al., 2021), but challenges still exist. Currently, medical staff shortages and backlogs of patients needing to catch up on preventive services lead to longer wait times for scheduling appointments and decreased screening rates (Smith and Perkins, 2022; Massad, 2022; Wentzensen et al., 2021). Little work has explored the impact of the COVID-19 pandemic on clinician perceptions of cervical cancer screening and staffing challenges in FQHCs. In order to identify characteristics that could be targets for future interventions or additional supports, this paper examines the association of clinician characteristics with perceived changes in cervical cancer screening and the impact of pandemic-related staffing changes on screening and abnormal results follow-up during the pandemic period of October 2021 through July 2022 in FQHCs and safety net settings of care. Methods Participant recruitment and target population The target population were clinicians, defined for the purpose of this study as physicians and Advanced Practice Providers (APPs), who conducted cervical cancer screening in federally qualified health centers and safety net settings of care (hereafter referred to as ‘FQHCs’) in the United States during the post-acute phase of the COVID-19 pandemic. Clinicians were eligible to participate if they: (1) performed cervical cancer screening, (2) were a physician or APP, and (3) were currently practicing in an FQHC in the US between October 2021 and July 2022, the post-acute period of the pandemic in the US when COVID-19 vaccination was widely available to the general population. We recruited clinicians for participation in the online survey hosted via Qualtrics through periodic recruitment email messages via the American Cancer Society Vaccinating Adolescents Against Cancer (VACs) program and the professional networks of the PIs (RBP, STV). Survey participants were asked if they would also be willing to participate in qualitative interviews via phone. A random sample of those who indicated willingness were contacted for participation. This study was approved by Moffitt Cancer Center’s Scientific Review Committee and Institutional Review Board (MCC #20048) and Boston University Medical Center’s Institutional Review Board (H-41533). All survey participants viewed an information sheet in lieu of reading and signing an informed consent form, and interview participants provided verbal consent. All were compensated for their time completing the survey or interview. Survey development and validation Quantitative survey questions were developed based on recent literature exploring the effects of the COVID-19 pandemic on cancer screening practices (Miller et al., 2021; Wentzensen et al., 2021) and the investigators’ clinical observations. The draft survey was reviewed by an expert panel of FQHC providers (n=8), refined, piloted, and finalized after incorporating pilot feedback and testing technical functionality of the Qualtrics survey among the study team. Clinician characteristics assessed included age, race/ethnicity, training, specialty, and geographic region. Age was measured in years and categorized for analysis as <30, 30–39, 40–49, 50+. Gender identity was assessed as male, female, transgender, and other. Race was assessed as Asian, Black/African American, White, Mixed race, Native Hawaiian/Pacific Islander, American Indian/Alaska Native, and Other. Ethnicity was assessed as Hispanic/Latinx or non-Hispanic/Latinx. Race/ethnicity was categorized for analysis as White non-Hispanic versus all others due to small cell sizes of non-White and Hispanic participants. For all variables assessed in this manuscript that allowed write-in/free responses, responses were re-classified within the pre-determined categories for each variable when possible. Clinician training was assessed as physician (medical doctor [MD], doctor of osteopathic medicine [DO]) or advanced practice providers (APPs) (physician assistant [PA], nurse practitioner [NP], and certified nurse midwife [CNM]). Clinician training was categorized as: (1) MD/DO (doctors of medicine and osteopathic medicine) and (2) APPs (NPs, CNMs, PAs). Clinical specialty was assessed as Obstetrics and Gynecology (OBGYN), family medicine, internal medicine (IM), pediatric/adolescent medicine, women’s health, and other (via write in). Based on prior literarature (Neugut et al., 2019) and the number of respondents in each category, we created the following categories for clinician specialty: (1) Women’s Health/OBGYN, (2) Family Medicine, and (3) IM, Pediatrics/Adolescent Medicine. Geographic location included four US regions (Northeast, South, Midwest, West) and a non-responder category for those who did not provide state or zip code. Based on national data indicating geographic variation in coverage rates by US region (Buskwofie et al., 2020) as well and distribution of respondents, region was categorized as (1) Northeast, (2) South, and (3) West and Midwest. We also assessed clinical behaviors and attitudes associated with cervical cancer screening. Questions captured the number of screens performed monthly, test(s) used for screening, attitudes toward using self-collected HPV testing for cervical cancer screening, barriers to screening, tracking systems, and staffing changes. Qualitative interview guide questions were developed based on recent literature (Miller et al., 2021; Wentzensen et al., 2021) and the investigators’ clinical observations. The draft interview guide was reviewed by an expert panel of FQHC providers (n=8) and revised. Interview questions explored survey topics in depth, including experiences with providing cervical cancer screening at different points during the pandemic, barriers to providing care, as well as strategies for improving follow-up, including tracking systems and self-sampled HPV testing. Data analysis Quantitative survey data We assessed descriptive statistics (frequencies, percentages) of clinician characteristics and outcome variables. We conducted separate exact binary logistic regressions (due to small cell sizes) examining the associations of clinician characteristics with (a) screening practices at the time of survey participation (the same/more versus less than pre-pandemic), and (b) pandemic-associated staffing changes impacting the ability to screen or follow-up (yes/no). The following variables were included in the full models for each outcome: race/ethnicity, age, gender, region, clinician training., clinician specialty. We used manual forward selection with a value for entry and significance of 0.10 because this strikes a balance between the commonly accepted method of using AIC (which assumes significance level of 0.157), and the often used alpha of 0.05, which could lead to failure to identify associations due to small sample size. Variables were added sequentially with the variable with the lowest p-value below 0.10 added at each step. We produced forest plots displaying odds ratios and confidence intervals from this model (Figure 2). Analyses were conducted in SAS version 9.4. Qualitative interview data Interviews were conducted by three co-authors (RBP, AM, HBF) trained in qualitative methodology via video conference (Zoom); interviews were audio recorded and transcribed verbatim. Data were coded using thematic content analysis (Elo and Kyngäs, 2008). Based on the questions in the initial interview guide, a priori codes were developed and a codebook created to operationalize and define each code. The qualitative analysis team independently reviewed the data twice. The team hand coded the data with the initial codes and made notes on possible new codes in the first coding pass. Then, notes on possible new codes were discussed until consensus was reached. The codes were then revised and transcripts reviewed using the updated code categories. This second coding pass served to clean coding from the first coding pass and identify emergent themes not initially identified (Unknown, 1998). At least two coders reviewed each transcript. Discrepancies were resolved by discussion in weekly group meetings. A centralized shared data sheet was used for coding to facilitate communication across different institutions. Role of the funding source This study was funded by the American Cancer Society, who had no role in the study’s design, conduct, or reporting. Results Quantitative survey data A total of 159 potential participants viewed the online study information sheet and completed screening items; 11 were excluded due to ineligible clinical training (n=5) or not conducting cervical cancer screening (n=6). Data were cleaned and invalid surveys were removed. Invalid surveys included potential duplicate responses identified by repeat IP address, nonsensical write-in free responses, and those with numerous skipped items. Table 1 details clinician characteristics and screening practices of the final analytic sample (n=148). Figure 1 provides a flow diagram describing the process of determining the final analytic sample size. The sample was primarily female (85%), White (70%), non-Hispanic (86%), and practiced in the Northeast (63%). Most (70%) reported specializing in family medicine, 19% reported Women’s Health/OBGYN, and 11% reported other specialties. All but one participant (99%) used Pap/HPV co-testing for routine screening of patients aged 30–65, and 61% performed 10 or fewer screens per month. Most (93%) clinicians determined the next step in management themselves when their patients had abnormal results (rather than refer to a specialist). Most (78%) had colposcopy available on site, though only 31% of participants reported that treatment (Loop Electrosurgical Excision Procedure, [LEEP]) was available on site. Table 1 Clinician characteristics and screening practices. VariableFrequency%Valid NClinician characteristicsAge147Less than 30201430–39563840–49362450+3524Gender identityFemale*12585148Male2215Transgender/gender non-binary10.67Race148Asian139Black/African American1510Mixed race107Other75White10370Ethnicity148Hispanic/Latinx2114Not Hispanic/Latinx12786Clinician Training148MD and DO6745APPs†8155Clinician Specialty148Women’s Health and Ob/GYN2819Family Medicine10370Internal Medicine, Pediatric/Adolescent Medicine, and ‘other’1711Region148Northeast9363South2819West & Midwest2618Non-responders10.7Current number of cervical cancer screenings performed per month1–10906111–202718>203121Pap/HPV co-testing as screening method for patients aged 30–65147 ‡99148Respondent determines management following abnormal results (yes)13893148Health center provides colposcopy on site (yes)11578148Health center provides treatment (LEEP) on site (yes)4631148PANDEMIC IMPACT ON SCREENING AND MANAGEMENTScreening in 2020 compared to pre-pandemic (less) §12795134Screening services stopped at any time during the pandemic (yes) §6653125Colposcopy services stopped at any time during the pandemic (yes) §, ¶3631115LEEP services stopped at any time during the pandemic (yes) §, ¶81746Screening in 2021/now compared to pre-pandemic §140Less3928Same6546More3626 *for all percentages included in all tables, when percentages were .6-.9, we rounded up to the next whole number. * Due to small numbers, transgender/non-binary/other were unable to be analyzed as their own category. They were assigned to female for regression analyses because female was the most common response. No difference was noted when grouped with male. † APPs included: NPs (52), CNMs (7), PAs (17), and other (5). ‡ The remaining respondent used primary HPV testing. No respondents in this sample used cytology alone. § Participants who selected ‘unsure’ were excluded from the denominator. 14 (9%) participants were unsure whether screening was less in 2020 compared to pre-pandemic, 23 (16%) were unsure whether screening services were stopped at any time, 53 participants (36%) were unsure whether colposcopy practices were stopped, 21 (14%) were unsure whether LEEP services were stopped, and 8 (5%) were unsure whether they were screening more or less in 2021/now compared to pre-pandemic. ¶ Participants who did not indicate that they performed colposcopy and LEEP services on site were excluded from the demonimator. Figure 1 Download asset Open asset Study flow chart depicting participant exclusions and final analytic sample. Most (95%) reported decreased screening during 2020 compared to pre-pandemic, and 53% stated that screening services were completely suspended at some point during the pandemic. Smaller proportions reported suspensions of colposcopy (31%) and LEEP (17%) services. By October 2021-July 2022, when the survey was conducted, screening had recovered somewhat. Approximately one-quarter (28%) reported less cervical cancer screening currently than before the pandemic, 46% reported the same amount, and 26% more screening. Among clinics providing LEEP services, 76% had currently resumed pre-pandemic LEEP capacity (data not shown). We examined cervical cancer screenings performed monthly by clinician training and specialty (Table 2). Overall, 32% of clinicians screened 1–5 patients monthly, 29% screened 6–10 patients, 18% screened 11–20 patients, and 21% reported screening >20 patients. Approximately 18% of MD/DOs and 23% of APPs screened >20 patients per month, while 37% of MD/DOs and 27% of APPs screened 1–5 patients per month. Screening practices varied by specialty, with 59% of clinicians in OBGYN/Women’s Health screening >20 patients per month compared to 11% in Family Medicine. Table 2 Cervical cancer screenings performed monthly by clinician specialty and clinician training. 1–5 patients per monthN=476–10 patients per monthN=4311–20 patients per monthN=27>20 patients per monthN=31TotalN=148Clinician TrainingMD/DO25 (37%)20 (30%)10 (15%)12 (18%)67APPs22 (27%)23 (28%)17 (21%)19 (23%)81Clinician SpecialtyOBGYN/Women’s Health2 (7%)4 (14%)6 (21%)17 (59%)29Family Medicine39 (38%)34 (33%)19 (18%)11 (11%)103IM, Peds/Adol. Med.6 (38%)5 (31%)2 (13%)3 (19%)16 Placeholder for Figure 1*Study flow chart depicting participant exclusions and final analytic sample. Table 3 and Figure 2 detail logistic regression model results for clinician and practice characteristics associated with odds of doing the same amount or more cervical cancer screening at the time of survey completion (2021–2022) as compared to before the COVID-19 pandemic. Region, gender, and age were not included in the model after completing the specified variable selection process. Clinician specialty was significantly associated with odds of doing the same or more cervical cancer screening at time of the survey (2021–2022) than before the pandemic (p=0.04). Compared to Women’s Health/OBGYNs, those who identified as family medicine clinicians and other were significantly associated with decreased odds of performing the same or more screening at time of survey (2021–22) (Family medicine: OR = 0.29, 95% CI: 0.08–1.07, p=0.06; Other: OR = 0.12, 95% CI: 0.025–0.606, p=0.01). Further, clinician training was significantly associated with increased odds of doing the same or more screening at time of the survey (2021–2022) as compared to before the pandemic (p = 0.06); compared to MDs/DOs, APPs had higher odds of performing the same or more screening at time of the survey (2021–2022) (OR = 2.15, 95% CI: 0.967–4.80, p=0.06). Clinician race/ethnicity was also significantly with non-White clinicians more to the same or more screening at time of the survey (2021–2022) as compared to White non-Hispanic clinicians (OR = 95% Table 3 model of clinician and practice characteristics associated with odds of conducting the same amount or more cervical cancer screening 2021 than before the COVID-19 pandemic selection was and the following variables were not selected for the final model (1) region (2) and (3) odds Family Peds/Adol. Women’s All other White reported is for for Figure plots depicting clinician and practice characteristics associated with odds of conducting the same or more cervical cancer screening 2021 before the pandemic. Figure 2 Download asset Open asset plots depicting clinician & practice characteristics associated with odds of conducting the same amount or more cervical cancer screening 2021 before the pandemic. Clinicians reported barriers to cervical cancer screening (Table The following were considered barriers by in-person availability patients not scheduling or appointments switching to and the to address more health was pandemic-associated staffing changes impacting the ability to screen for cervical track abnormal or follow-up with their patients, which was reported by of participants. Approximately half of participants reported decreased staffing of medical and staff as compared to pre-pandemic while one reported in physicians APPs and reported lack of health was an to screening. Table to cervical cancer screening and strategies for tracking patients. barriers in-person availability at health (3) not scheduling not appointments (3) lack of health or to track patients who are due for Health center providers) not screening due to to address more health to visits screening not staffing changes impacted ability to screen or track abnormal results health center staffing compared to the other Advanced Practice Medical * Participants were also asked of patients were unable to treatment (LEEP) due to Clinician and practice characteristics associated with odds of staff tracking abnormal and follow-up were also assessed using logistic In manual gender, region, age, race/ethnicity, clinician specialty and training were not selected for the final indicating no significantly associated with staffing Table results to strategies for tracking patient screening and abnormal address care during the pandemic, most participants reported scheduling screening at the time of visits performing screening when patients for other and medical reported clinical or to screening. A reported that they did not have any to track patients overdue for screening. The most commonly reported tracking systems for screening included the medical and staff asked management of abnormal screening participants most commonly reported that they were not of a tracking systems were in they included: medical tracking a staff and paper Table for tracking patients and up on or for up on screenings that were due to the via are for future screening medical is to identify patients who are cervical cancer screening to perform cervical cancer screening at of to screen during for tracking patients overdue for of any of has own medical staff to review and for tracking abnormal results colposcopy of has own not of any own medical staff person to review and participants were asked to all that to HPV self-sampling has as a method to improve cervical cancer screening Table clinician attitudes HPV self-sampling as a A total of 31% felt that self-sampling would be very helpful and 61% felt would be somewhat helpful to address pandemic-associated screening Approximately half would self-sampling only to patients who were unable to screening, would to any patient who to would self-sampling for all patients, and would not self-sampling. The most common perceived of self-sampling were screening patients who had or screening patients who had access to care However, clinicians reported patients not in a or not for other primary care services 31% Participants were to free text to their in this participants who HPV self-sampling experiences with rates and in cancer screening. Table HPV self-sampling perceptions and practices. of HPV self-sampling to catch up patients overdue for screening due to COVID-19 HPV self-sampling of sample for cervical cancer patient who a over a who have screening in because of fear of to with would not HPV to perform HPV in or on of self-sampled HPV a

Source: eLife

DOI: 10.7554/elife.86358.sa2