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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

  1. Lindsay Fuzzell  Is a corresponding author
  2. Paige Lake  Is a corresponding author
  3. Naomi C Brownstein
  4. Holly B Fontenot
  5. Ashley Whitmer
  6. Alexandra Michel
  7. McKenzie McIntyre
  8. Sarah L Rossi
  9. Sidika Kajtezovic
  10. Susan T Vadaparampil
  11. Rebecca Perkins
  1. H. Lee Moffitt Cancer Center & Research Institute, Health Outcomes and Behavior, United States
  2. Medical University of South Carolina, Public Health Sciences, United States
  3. University of Hawaii at Manoa, Nancy Atmospera-Walch School of Nursing, United States
  4. Boston University, Chobanian & Avedisian School of Medicine, United States
  5. H. Lee Moffitt Cancer Center & Research Institute, Office of Community Outreach, Engagement, and Equity, United States
https://doi.org/10.7554/eLife.86358
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Cite this article
  1. Lindsay Fuzzell
  2. Paige Lake
  3. Naomi C Brownstein
  4. Holly B Fontenot
  5. Ashley Whitmer
  6. Alexandra Michel
  7. McKenzie McIntyre
  8. Sarah L Rossi
  9. Sidika Kajtezovic
  10. Susan T Vadaparampil
  11. Rebecca Perkins
(2023)
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
eLife 12:e86358.
https://doi.org/10.7554/eLife.86358
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2 figures, 7 tables and 2 additional files

Figures

Figure 1
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Study flow chart depicting participant exclusions and final analytic sample.
Figure 2
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Forest plots depicting clinician & practice characteristics associated with odds of reporting conducting the same amount or more cervical cancer screening now/in 2021 vs before the pandemic.

Tables

Table 1
Clinician characteristics and screening practices.
VariableFrequency%Valid N
Clinician characteristics
Age147
Less than 302014
30–395638
40–493624
50+3524
Gender identity
Female*12585148
Male2215
Transgender/gender non-binary10.67
Race148
Asian139
Black/African American1510
Mixed race107
Other75
White10370
Ethnicity148
Hispanic/Latinx2114
Not Hispanic/Latinx12786
Clinician Training148
MD and DO6745
APPs†8155
Clinician Specialty148
Women’s Health and Ob/GYN2819
Family Medicine10370
Internal Medicine, Pediatric/Adolescent Medicine, and ‘other’1711
Region148
Northeast9363
South2819
West & Midwest2618
Non-responders10.7
Current number of cervical cancer screenings performed per month
1–109061
11–202718
>203121
Pap/HPV co-testing as screening method for patients aged 30–65147 ‡99148
Respondent determines management following abnormal results (yes)13893148
Health center provides colposcopy on site (yes)11578148
Health center provides treatment (LEEP) on site (yes)4631148
PANDEMIC IMPACT ON SCREENING AND MANAGEMENT
Screening in 2020 compared to pre-pandemic (less) §12795134
Screening services stopped at any time during the pandemic (yes) §6653125
Colposcopy services stopped at any time during the pandemic (yes) §, 3631115
LEEP services stopped at any time during the pandemic (yes) §, 81746
Screening in 2021/now compared to pre-pandemic §140
Less3928
Same6546
More3626

  1. *for all percentages included in all tables, when percentages were .6-.9, we rounded up to the next whole number.

  2. *

    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.

  3. †

    APPs included: NPs (52), CNMs (7), PAs (17), and other (5).

  4. ‡

    The remaining respondent used primary HPV testing. No respondents in this sample used cytology alone.

  5. §

    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.

  6. Participants who did not indicate that they performed colposcopy and LEEP services on site were excluded from the demonimator.

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=148
Clinician Training
MD/DO25 (37%)20 (30%)10 (15%)12 (18%)67
APPs22 (27%)23 (28%)17 (21%)19 (23%)81
Clinician Specialty
OBGYN/Women’s Health2 (7%)4 (14%)6 (21%)17 (59%)29
Family Medicine39 (38%)34 (33%)19 (18%)11 (11%)103
IM, Peds/Adol. Med.6 (38%)5 (31%)2 (13%)3 (19%)16

  1. Placeholder for Figure 1*Study flow chart depicting participant exclusions and final analytic sample.

Table 3
Final model of clinician and practice characteristics associated with odds of reporting conducting the same amount or more cervical cancer screening now/in 2021 than before the COVID-19 pandemic (N=140).

Manual forwards selection was utilized and the following variables were not selected for the final model (p>0.10): (1) region (2) gender and (3) age.

Overall pBSEAdjusted odds ratiopCI
Clinician training0.0605
 APPs0.76760.40892.1550.06050.967–4.802
 MD/DO-----
Clinician specialty0.0364
 Family Medicine–1.22140.65940.2950.06400.081–1.07
 Int. Med., Peds/Adol. Med.–2.09960.81590.1230.01010.025-.606
 Women’s Health/OBGYN-----
Clinician race/ethnicity0.0873
 All other races/ethnicities0.76940.45002.11590.08730.894–5.214
 White non-Hispanic-----

  1. *CI reported is for OR.

  2. *Placeholder for Figure 2* Forest plots depicting clinician and practice characteristics associated with odds of reporting conducting the same or more cervical cancer screening now/in 2021 vs. before the pandemic.

Table 4
Barriers to cervical cancer screening and strategies for tracking patients.
BARRIERSRarelyn (%)Sometimesn (%)Oftenn (%)Unsuren (%)Valid N
Systems barriers    148
Limited in-person appointment availability at our health center24 (16)53 (36)66 (45)5 (3) 
Patients not scheduling appointments5 (3)50 (34)85 (57)8 (6) 
Patients not attending appointments (no shows)8 (6)73 (49)62 (42)5 (3) 
Patient lack of health insurance or limited coverage*83 (56)36 (24)18 (12)11 (8) 
Inability to track patients who are due for screening58 (39)46 (31)32 (22)12 (8) 
Health center (or providers) not prioritizing screening due to need to address more acute health problems34 (23)61 (41)46 (31)7 (5) 
Switched to telemedicine visits so screening not available34 (23)59 (40)48 (33)6 (4) 
Staffing barriersFrequencyPercent148
COVID-related staffing changes impacted ability to screen or track abnormal results (yes)6745 
Current health center staffing compared to pre-pandemicDecreased
n (%)		Stayed the same
n (%)		Increased
n (%)		Unsure
n (%)		148
Physician (MD, DO)52 (35)80 (54)6 (4)10 (7) 
Nurse practitioner, Physician Assistant, Certified Nurse Midwife, other Advanced Practice Provider42 (28)71 (48)22 (15)13 (9) 
Nurse (RN, LPN)42 (28)71 (48)22 (15)13 (9) 
Medical Assistant83 (56)45 (30)8 (6)12 (8) 
Office Staff64 (43)64 (43)6 (4)14 (10) 
  1. *

    Participants were also asked what proportion of patients were unable to obtain treatment (LEEP) due to financial issues, 70% (n=102) answered 0–20%.

Table 5
Strategies for tracking patients and catching up on missed screenings*.
STRATEGIESFrequencyPercentValid N
Policies or plans for catching up on screenings that were missed due to the pandemic148
Patients seen via telemedicine are scheduled for future screening visits11074
Electronic medical record is queried to identify patients who are overdue9262
Added dedicated cervical cancer screening days/hours3222
Try to perform cervical cancer screening at acute problem visits/take advantage of opportunities to screen during unrelated visits9061
System for tracking patients overdue for screening148
No, unaware of any system2920
Paper log of patients53
Each dept. has its own system53
Electronic medical record tracker9463
Dedicated staff person/team member to review records and contact patients3725
Other1611
System for tracking abnormal results (e.g., colposcopy referrals)148
Paper log of patients85
Each dept. has its own system75
I am not aware of any system/each provider tracks own results5638
Electronic medical record tracker5034
Dedicated staff person to review records and contact patients5336
Other1611

  1. Note, participants were asked to check all that apply therefore answers sum to >100%.

Table 6
HPV self-sampling perceptions and practices.
Frequency%Valid N
Helpfulness of HPV self-sampling to catch up patients overdue for screening due to COVID-19 pandemic147
Not helpful128
Somewhat helpful8961
Very helpful4631
Would recommend HPV self-sampling instead of clinician-collected sample for cervical cancer screening148
All patients96
Any patient who preferred a self-sample over a clinician-collected sample5235
Only pts. who couldn’t have screening in clinic because of transportation issues, fear of coming to clinic, difficulty with speculum exams7249
N/A I would not offer HPV self-sampling85
Other75
Location to perform self-sample HPV tests148
In clinic86
At home96
Either in clinic or home, depending on pt. preference12086
Other32
Benefits/advantages of self-sampled HPV testingNot a benefit
n (%)		Small benefit
n (%)		Moderate benefit
n (%)		Large benefit
n (%)		147
Screen patients who have difficulty accessing screening due to lack of qualified providers, distance to clinic, or logistical barriers (e.g., childcare or work schedules)7 (5)32 (22)50 (34)58 (39)
Screen patients via telemedicine10 (7)50 (34)44 (30)43 (29)
Screen patients who would prefer not to have speculum exams (e.g. mobility issues or history of trauma)3 (2)23 (16)38 (26)83 (56)
Concerns about self-sampled HPV testingNot a concernSmall concernModer-ate concernLarge concern147
A pelvic exam by a clinician should be part of cervical cancer screening20 (13)57 (39)38 (26)32 (22)
Patients may not collect adequate specimens4 (3)45 (31)49 (33)49 (33)
Patient may not return specimen in a timely manner3 (2)37 (25)51 (35)56 (38)
If performed at home, patients may not present for routine primary care or follow-up for abnormal test results13 (9)39 (27)49 (33)46 (31)
Table 7
Qualitative themes with exemplar quotes.
ThemeExemplar quotes
Initial pandemic-associated barriers“I would say it definitely disrupted all the cancer screenings, the mammo[gram]’s, the colonoscopies, the pap smears, I would say for the whole year of 2020 into about March of 2021.” (APP, Family Medicine)
“We were only doing acute visits… everything else was by phone.” (MD, Family Medicine)
Ongoing barriers (system and staffing)System-related:
“We have the EMR triggering, and we have active tracking of abnormal Paps. But as far as getting people in for their routine screening, I don't believe we have someone actively tracking that. I feel like it’s more on the provider picking it up as they open the chart.” (APP, Family Medicine)
Staffing-related:
“We are still working with reduced staff in the office. So, there are definitely still much fewer appointments available.” (APP, Family Medicine)
“We realized … we really need to start doing colposcopy again. But unfortunately, that’s also when our physician colposcopy provider left.” (MD/DO, Family Medicine)
“Rates of burnout, and then the competition from other systems, hiring people away was pretty debilitating at times.” (APP, Family Medicine)
Facilitators and strategies for catching up on cervical cancer screeningStaffing and tracking:
“Patients get reminders… the health center as a whole has been trying to run lists of people that are due and bring them in.” (APP, Family Medicine)
“If they had an abnormal PAP, the nursing staff would have ticklers [in the EMR] created as a reminder that it’s time for the patient to have a PAP… We have two nurses who are dedicated not for just PAP tracking but for general ticklers.” (MD/DO, Internal Medicine).
HPV self-sampling benefits:
“It decreases any concerns for like privacy, for discomfort, you know, patients who have trauma histories, maybe patients who are transgender, patients who, you know, like I said, work schedules don't allow them to get in on time, um, it just opens up a way for them to still all be screened in a way that can hopefully feel comfortable and accessible.” (APP, OBGYN/Women’s Health)
“I think it could be [useful to address pandemic-related screening deficits]. Especially if we don't have, um, as many in-person appointments available.” (APP, Family Medicine)
HPV self-sampling concerns:
Inadequate sample:
“Making sure that people you know, kind of collect it correctly, mostly just because in my experience, people have not great knowledge about their own anatomy sometimes… if somebody accidentally puts the swab in their rectum, instead of the vagina, you would probably get an HPV result, because you can do HPV testing in the rectum, but you're not getting a, a cervical cancer screening.” (APP, OBGYN/Women’s Health)
Kits will not be returned:
“We do our –occult blood sampling with home tests, and sometimes –many times, those kits go home and never come back. We're always chasing a patient to kind of get them to bring it back or mail it back.” (APP, Family Medicine)

Additional files

MDAR checklist
https://cdn.elifesciences.org/articles/86358/elife-86358-mdarchecklist1-v1.docx
Reporting standard 1
https://cdn.elifesciences.org/articles/86358/elife-86358-repstand1-v1.docx

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  1. Lindsay Fuzzell
  2. Paige Lake
  3. Naomi C Brownstein
  4. Holly B Fontenot
  5. Ashley Whitmer
  6. Alexandra Michel
  7. McKenzie McIntyre
  8. Sarah L Rossi
  9. Sidika Kajtezovic
  10. Susan T Vadaparampil
  11. Rebecca Perkins
(2023)
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
eLife 12:e86358.
https://doi.org/10.7554/eLife.86358