Research Article

Computational and Systems Biology

A model-based analysis of the health impacts of COVID-19 disruptions to primary cervical screening by time since last screen for current and future disruptions

Center for Health Decision Science, Harvard T.H. Chan School of Public Health, United States
Department of Health Management and Health Economics, University of Oslo, Norway
Department of Public Health, Erasmus MC, University Medical Center Rotterdam, Netherlands
Centre for Health Policy & Management, School of Medicine, Trinity College Dublin, Ireland
Faculty of Life Sciences & Medicine, School of Cancer & Pharmaceutical Sciences, King’s College London, United Kingdom
Cancer Research Division, Cancer Council NSW, Australia
Hokkaido University Center for Environmental and Health Sciences, Japan
Daffodil Centre, University of Sydney, a joint venture with Cancer Council NSW, Australia

Oct 12, 2022

https://doi.org/10.7554/eLife.81711

Open access
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Figures
Tables
Additional files

5 figures, 5 tables and 1 additional file

Figures

Figure 1

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Scenario overview reflecting the heterogeneity in screening history (aligned so that 2020 was 1, 3, 5, or 10 years since their last screen) facing alternative COVID-19 delay disruptions for three birth cohorts of women.

Figure 2

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Short-term impacts: relative rate ratio of cancer detected during the screening delay period for underscreeners compared with the same delay duration for guidelines-compliant screeners.

Figure 3

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Long-term impacts: projected impact of COVID-19-related disruptions to primary cervical cancer screening on the lifetime risk of developing cervical cancer (averaged across the 1965/1975/1985 birth cohorts of women) by time since last screen for cytology-based screening (top panels) and human papillomavirus (HPV)-based screening (bottom panels) for three Cancer Intervention and Surveillance Modeling Network (CISNET-Cervical disease simulation models).

Figure 4

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Long-term impacts: projected impact of COVID-19-related disruptions to primary cervical cancer screening on the incremental lifetime risk of developing cervical cancer (averaged across the 1965/1975/1985 birth cohorts of women) by time since last screen for cytology-based screening (top panels) and human papillomavirus (HPV)-based screening (bottom panels) for three Cancer Intervention and Surveillance Modeling Network (CISNET)-Cervical disease simulation models.

Appendix 1—figure 1

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Schematic of short-term cancer burden calculations*.

Tables

Table 1

Long-term health impacts* of a 5-year temporary delay to screening compared with no delay, by screening history, that is, screening frequency.

	Screening frequency
	Annual	3-yearly	5-yearly	10-yearly^†
Primary cytology-based screening
Harvard
Absolute change in lifetime risk	0.008%	0.022%	0.031%	0.044%
Excess cases over lifetime per 100,000 women	8	22	31	44
MISCAN-Cervix
Absolute change in lifetime risk	0.021%	0.031%	0.034%	0.047%
Excess cases over lifetime per 100,000 women	21	31	34	47
Policy1-Cervix
Absolute change in lifetime risk	0.014%	0.020%	0.029%	0.066%
Excess cases over lifetime per 100,000 women	14	20	28	66
Primary HPV-based screening
Harvard
Absolute change in lifetime risk	0.000%	0.001%	0.004%	0.040%
Excess cases over lifetime per 100,000 women	0	1	4	40
MISCAN-Cervix
Absolute change in lifetime risk	0.017%	0.032%	0.041%	0.063%
Excess cases over lifetime per 100,000 women	17	32	41	63
Policy1-Cervix
Absolute change in lifetime risk	0.000%	0.006%	0.012%	0.058%
Excess cases over lifetime per 100,000 women	0	6	12	58

*

Risks are rounded to nearest 0.001%.
†

The women born in 1985 (aged 35 in 2020) received their last screen at age 25 and have not yet made the switch to primary human papillomavirus (HPV)-based screening. In the primary HPV-based analysis, these women would switch to primary HPV-based screening for their remaining lifetime either at 35 (under the no delay scenario) or aged >35 years (with a delay).

Appendix 1—table 1

Screening end age (lifetime number of screens) by birth cohort, screening frequency, and delay duration.

		Annual	3-yearly*	5-yearly^†	10-yearly
1965 (age 55 in 2020)	No delay	65 (45)	64 (15)	65 (9)	65 (5)
	1-year delay	65 (44)	65 (15)	61 (8)	56 (4)
	2-year delay	65 (43)	63 (14)	62 (8)	57 (4)
	5-year delay	65 (40)	63 (13)	65 (8)	60 (4)
1975 (age 45 in 2020)	No delay	65 (45)	63 (15)	65 (9)	65 (5)
	1-year delay	65 (44)	64 (15)	61 (8)	56 (4)
	2-year delay	65 (43)	65 (15)	62 (8)	57 (4)
	5-year delay	65 (40)	65 (14)	65 (8)	60 (4)
1985 (age 35 in 2020)	No delay	65 (45)	65 (15)	65 (8)	65 (5)
	1-year delay	65 (44)	63 (14)	61 (8)	56 (4)
	2-year delay	65 (43)	64 (14)	62 (8)	57 (4)
	5-year delay	65 (40)	64 (13)	65 (8)	60 (4)

*

Guidelines-compliant screener with primary cytology-based screening.
†

Guidelines-compliant screener with primary human papillomavirus (HPV) testing for women aged 30+ years.

Appendix 1—table 2

Example age at screen for the 1975 birth cohort without (highlighted in green) and with (highlighted in yellow) COVID-19-related delays by screening frequency.

Numbers under each delay are ages, bolded numbers are ages at which screening takes place, green highlight reflects no delay, and yellow highlights reflects a delay.

	No delay					1-year delay					2-year delay					5-year delay
Year	Q1	Q3	Q5	Q10	Year	Q1	Q3	Q5	Q10	Year	Q1	Q3	Q5	Q10	Year	Q1	Q3	Q5	Q10
1996	21	21	21	21	1996	21	21	21	21	1996	21	21	21	21	1996	21	21	21	21
1997	22	22	22	22	1997	22	22	22	22	1997	22	22	22	22	1997	22	22	22	22
1998	23	23	23	23	1998	23	23	23	23	1998	23	23	23	23	1998	23	23	23	23
1999	24	24	24	24	1999	24	24	24	24	1999	24	24	24	24	1999	24	24	24	24
2000	25	25	25	25	2000	25	25	25	25	2000	25	25	25	25	2000	25	25	25	25
2001	26	26	26	26	2001	26	26	26	26	2001	26	26	26	26	2001	26	26	26	26
2002	27	27	27	27	2002	27	27	27	27	2002	27	27	27	27	2002	27	27	27	27
2003	28	28	28	28	2003	28	28	28	28	2003	28	28	28	28	2003	28	28	28	28
2004	29	29	29	29	2004	29	29	29	29	2004	29	29	29	29	2004	29	29	29	29
2005	30	30	30	30	2005	30	30	30	30	2005	30	30	30	30	2005	30	30	30	30
2006	31	31	31	31	2006	31	31	31	31	2006	31	31	31	31	2006	31	31	31	31
2007	32	32	32	32	2007	32	32	32	32	2007	32	32	32	32	2007	32	32	32	32
2008	33	33	33	33	2008	33	33	33	33	2008	33	33	33	33	2008	33	33	33	33
2009	34	34	34	34	2009	34	34	34	34	2009	34	34	34	34	2009	34	34	34	34
2010	35	35	35	35	2010	35	35	35	35	2010	35	35	35	35	2010	35	35	35	35
2011	36	36	36	36	2011	36	36	36	36	2011	36	36	36	36	2011	36	36	36	36
2012	37	37	37	37	2012	37	37	37	37	2012	37	37	37	37	2012	37	37	37	37
2013	38	38	38	38	2013	38	38	38	38	2013	38	38	38	38	2013	38	38	38	38
2014	39	39	39	39	2014	39	39	39	39	2014	39	39	39	39	2014	39	39	39	39
2015	40	40	40	40	2015	40	40	40	40	2015	40	40	40	40	2015	40	40	40	40
2016	41	41	41	41	2016	41	41	41	41	2016	41	41	41	41	2016	41	41	41	41
2017	42	42	42	42	2017	42	42	42	42	2017	42	42	42	42	2017	42	42	42	42
2018	43	43	43	43	2018	43	43	43	43	2018	43	43	43	43	2018	43	43	43	43
2019	44	44	44	44	2019	44	44	44	44	2019	44	44	44	44	2019	44	44	44	44
2020	45	45	45	45	2020	45	45	45	45	2020	45	45	45	45	2020	45	45	45	45
2021	46	46	46	46	2021	46	46	46	46	2021	46	46	46	46	2021	46	46	46	46
2022	47	47	47	47	2022	47	47	47	47	2022	47	47	47	47	2022	47	47	47	47
2023	48	48	48	48	2023	48	48	48	48	2023	48	48	48	48	2023	48	48	48	48
2024	49	49	49	49	2024	49	49	49	49	2024	49	49	49	49	2024	49	49	49	49
2025	50	50	50	50	2025	50	50	50	50	2025	50	50	50	50	2025	50	50	50	50
2026	51	51	51	51	2026	51	51	51	51	2026	51	51	51	51	2026	51	51	51	51
2027	52	52	52	52	2027	52	52	52	52	2027	52	52	52	52	2027	52	52	52	52
2028	53	53	53	53	2028	53	53	53	53	2028	53	53	53	53	2028	53	53	53	53
2029	54	54	54	54	2029	54	54	54	54	2029	54	54	54	54	2029	54	54	54	54
2030	55	55	55	55	2030	55	55	55	55	2030	55	55	55	55	2030	55	55	55	55
2031	56	56	56	56	2031	56	56	56	56	2031	56	56	56	56	2031	56	56	56	56
2032	57	57	57	57	2032	57	57	57	57	2032	57	57	57	57	2032	57	57	57	57
2033	58	58	58	58	2033	58	58	58	58	2033	58	58	58	58	2033	58	58	58	58
2034	59	59	59	59	2034	59	59	59	59	2034	59	59	59	59	2034	59	59	59	59
2035	60	60	60	60	2035	60	60	60	60	2035	60	60	60	60	2035	60	60	60	60
2036	61	61	61	61	2036	61	61	61	61	2036	61	61	61	61	2036	61	61	61	61
2037	62	62	62	62	2037	62	62	62	62	2037	62	62	62	62	2037	62	62	62	62
2038	63	63	63	63	2038	63	63	63	63	2038	63	63	63	63	2038	63	63	63	63
2039	64	64	64	64	2039	64	64	64	64	2039	64	64	64	64	2039	64	64	64	64
2040	65	65	65	65	2040	65	65	65	65	2040	65	65	65	65	2040	65	65	65	65
2041	66	66	66	66	2041	66	66	66	66	2041	66	66	66	66	2041	66	66	66	66

Appendix 1—table 3

Relative rate ratios and accumulated incidence rates per 100,000 women for each screening frequency and delay scenario.

Screening frequency	1-year delay	2-year delay	5-year delay
Policy1-Cervix
5-yearly screener (cytology)	1.40 = 4.94/3.58	1.44 = 10.05/7.00	1.57 = 30.03/19.10
10-yearly screener (cytology)	3.10 = 11.06/3.58	3.35 = 23.45/7.00	3.34 = 63.72/19.10
10-yearly screener (HPV)	2.26 = 7.36/3.26	2.48 = 15.31/6.18	2.54 = 42.41/16.67
MISCAN-Cervix
5-yearly screener (cytology)	2.78 = 3.00/1.08	2.28 = 6.41/2.81	1.99 = 22.09/11.08
10-yearly screener (cytology)	6.97 = 7.54/1.08	5.73 = 16.11/2.81	4.15 = 45.97/11.08
10-yearly screener (HPV)	3.91 = 6.08/1.55	3.67 = 13.08/3.56	2.97 = 38.84/13.09
Harvard
5-yearly screener (cytology)	1.8 = 9.64/5.37	1.74 = 17.69/10.15	1.64 = 45.97/27.96
10-yearly screener (cytology)	3.8 = 20.39/5.37	3.64 = 36.94/10.15	3.19 = 89.29/27.96
10-yearly screener (HPV)	3.61 = 10.74/2.98	3.58 = 19.51/5.45	3.69 = 46.83/12.68

Relative rate ratio is calculated as the accumulated incidence rate per 100,000 women during a delay period for a give screening history divided by the accumulated incidence rate per 100,000 women during the same delay period among guidelines-compliant screeners. Incidence rates are the average across the three birth cohorts. 3-yearly cytology screening is considered guidelines-compliant screening; 5-yearly human papillomavirus (HPV) screening is considered guidelines compliant.

Appendix 1—table 4

Percentage reduction in average (across the 1965, 1975, and 1985 birth cohorts) lifetime risk of cancer compared with no screening.

	Screening frequency
	Annual (%)	3-yearly (%)	5-yearly (%)	10-yearly (%)
Primary cytology-based screening
Harvard
No delay	88.4	79.9	71.4	56.3
1-year delay	88.5	80.0	70.9	55.3
2-year delay	88.4	79.5	70.5	54.9
5-year delay	87.9	78.4	69.3	53.4
MISCAN-Cervix
No delay	85.1	72.1	62.1	48.4
1-year delay	85.0	71.7	60.2	44.7
2-year delay	84.7	71.2	59.9	44.9
5year delay	83.1	69.1	58.8	43.9
Policy1-Cervix
No delay	87.7	86.5	84.5	75.9
1-year delay	87.8	86.3	82.3	71.9
2-year delay	87.7	85.8	82.5	71.9
5-year delay	86.8	85.1	82.5	71.3
Primary HPV-based screening
Harvard
No delay	92.6	89.3	86.7	77.8
1-year delay	92.6	89.4	86.6	77.1
2-year delay	92.6	89.4	86.6	76.7
5-year delay	92.6	89.2	86.4	75.0
MISCAN-Cervix
No delay	94.0	84.2	74.8	58.0
1-year delay	93.9	83.8	72.3	53.5
2-year delay	93.6	83.2	72.3	53.5
5-year delay	92.3	81.0	70.8	51.8
Policy1-Cervix
No delay	90.9	90.4	90.1	86.6
1-year delay	90.9	90.4	88.7	82.7
2-year delay	91.0	90.1	89.0	82.8
5-year delay	91.0	90.0	89.2	82.6

HPV, human papillomavirus.

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Emily A Burger
Inge MCM de Kok
James F O'Mahony
Matejka Rebolj
Erik EL Jansen
Daniel D de Bondt
James Killen
Sharon J Hanley
Alejandra Castanon
Mary Caroline Regan
Jane J Kim
Karen Canfell
Megan A Smith

(2022)

A model-based analysis of the health impacts of COVID-19 disruptions to primary cervical screening by time since last screen for current and future disruptions

eLife 11:e81711.

https://doi.org/10.7554/eLife.81711

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Scenario overview reflecting the heterogeneity in screening history (aligned so that 2020 was 1, 3, 5, or 10 years since their last screen) facing alternative COVID-19 delay disruptions for three birth cohorts of women.

Short-term impacts: relative rate ratio of cancer detected during the screening delay period for underscreeners compared with the same delay duration for guidelines-compliant screeners.

Schematic of short-term cancer burden calculations*.

Long-term health impacts* of a 5-year temporary delay to screening compared with no delay, by screening history, that is, screening frequency.

Screening end age (lifetime number of screens) by birth cohort, screening frequency, and delay duration.

Example age at screen for the 1975 birth cohort without (highlighted in green) and with (highlighted in yellow) COVID-19-related delays by screening frequency.

Relative rate ratios and accumulated incidence rates per 100,000 women for each screening frequency and delay scenario.

Percentage reduction in average (across the 1965, 1975, and 1985 birth cohorts) lifetime risk of cancer compared with no screening.

MDAR checklist

Downloads (link to download the article as PDF)

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Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)