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Published in: BMC Women's Health 1/2022

Open Access 01-12-2022 | Human Papillomavirus | Research

Colposcopy non-attendance following an abnormal cervical cancer screening result: a prospective population-based cohort study

Authors: Linda A. Liang, Sylke R. Zeissig, Gunther Schauberger, Sophie Merzweiler, Kathrin Radde, Sabine Fischbeck, Hans Ikenberg, Maria Blettner, Stefanie J. Klug

Published in: BMC Women's Health | Issue 1/2022

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Abstract

Background

A considerable proportion of cervical cancer diagnoses in high-income countries are due to lack of timely follow-up of an abnormal screening result. We estimated colposcopy non-attendance, examined the potential factors associated and described non-attendance reasons in a population-based screening study.

Methods

Data from the MARZY prospective cohort study were analysed. Co-test screen-positive women (atypical squamous cells of undetermined significance or worse [ASC-US+] or high-risk human papillomavirus [hrHPV] positive) aged 30 to 65 years were referred to colposcopy within two screening rounds (3-year interval). Women were surveyed for sociodemographic, HPV-related and other data, and interviewed for non-attendance reasons. Logistic regression was used to examine potential associations with colposcopy attendance.

Results

At baseline, 2,627 women were screened (screen-positive = 8.7%), and 2,093 again at follow-up (screen-positive = 5.1%; median 2.7 years later). All screen-positives were referred to colposcopy, however 28.9% did not attend despite active recall. Among co-test positives (ASC-US+ and hrHPV) and only hrHPV positives, 19.6% were non-attendees. Half of only ASC-US+ screenees attended colposcopy. Middle age (adjusted odds ratio [aOR] = 1.55, 95% CI 1.02, 4.96) and hrHPV positive result (aOR = 3.04, 95% CI 1.49, 7.22) were associated with attendance. Non-attendance was associated with having ≥ 3 children (aOR = 0.32, 95% CI 0.10, 0.86). Major reasons for non-attendance were lack of time, barriers such as travel time, need for childcare arrangements and the advice against colposcopy given by the gynaecologist who conducted screening.

Conclusions

Follow-up rates of abnormal screening results needs improvement. A systematic recall system integrating enhanced communication and addressing follow-up barriers may improve screening effectiveness.
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Literature
1.
go back to reference Maver PJ, Poljak M. Primary HPV-based cervical cancer screening in Europe: implementation status, challenges, and future plans. Clin Microbiol Infect. 2020;26(5):579–83.CrossRef Maver PJ, Poljak M. Primary HPV-based cervical cancer screening in Europe: implementation status, challenges, and future plans. Clin Microbiol Infect. 2020;26(5):579–83.CrossRef
3.
go back to reference Leyden WA, Manos MM, Geiger AM, Weinmann S, Mouchawar J, Bischoff K, et al. Cervical cancer in women with comprehensive health care access: attributable factors in the screening process. J Natl Cancer Inst. 2005;97(9):675–83.CrossRef Leyden WA, Manos MM, Geiger AM, Weinmann S, Mouchawar J, Bischoff K, et al. Cervical cancer in women with comprehensive health care access: attributable factors in the screening process. J Natl Cancer Inst. 2005;97(9):675–83.CrossRef
4.
go back to reference Doubeni CA, Gabler NB, Wheeler CM, McCarthy AM, Castle PE, Halm EA, et al. Timely follow-up of positive cancer screening results: a systematic review and recommendations from the PROSPR Consortium. CA Cancer J Clin. 2018;68(3):199–216.CrossRef Doubeni CA, Gabler NB, Wheeler CM, McCarthy AM, Castle PE, Halm EA, et al. Timely follow-up of positive cancer screening results: a systematic review and recommendations from the PROSPR Consortium. CA Cancer J Clin. 2018;68(3):199–216.CrossRef
5.
go back to reference Hillemanns P, Iftner T. New secondary prevention of cervical cancer in Germany starting in 2020. Onkologe. 2020;26(7):591–7.CrossRef Hillemanns P, Iftner T. New secondary prevention of cervical cancer in Germany starting in 2020. Onkologe. 2020;26(7):591–7.CrossRef
6.
go back to reference Klug SJ, Taylor KJ, Scheidemann-Wesp U, Lautz D, Guther B, Potthoff P, et al. Participation in cervical cancer screening in Germany. Prev Med. 2010;51(5):431–2.CrossRef Klug SJ, Taylor KJ, Scheidemann-Wesp U, Lautz D, Guther B, Potthoff P, et al. Participation in cervical cancer screening in Germany. Prev Med. 2010;51(5):431–2.CrossRef
7.
go back to reference Tanaka LF, Schriefer D, Radde K, Schauberger G, Klug SJ. Impact of opportunistic screening on squamous cell and adenocarcinoma of the cervix in Germany: A population-based case-control study. PLoS ONE. 2021;16(7): e0253801.CrossRef Tanaka LF, Schriefer D, Radde K, Schauberger G, Klug SJ. Impact of opportunistic screening on squamous cell and adenocarcinoma of the cervix in Germany: A population-based case-control study. PLoS ONE. 2021;16(7): e0253801.CrossRef
8.
go back to reference Marquardt K, Buttner HH, Broschewitz U, Barten M, Schneider V. Persistent carcinoma in cervical cancer screening: non-participation is the most significant cause. Acta Cytol. 2011;55(5):433–7.CrossRef Marquardt K, Buttner HH, Broschewitz U, Barten M, Schneider V. Persistent carcinoma in cervical cancer screening: non-participation is the most significant cause. Acta Cytol. 2011;55(5):433–7.CrossRef
9.
go back to reference Jordan J, Arbyn M, Martin-Hirsch P, Schenck U, Baldauf JJ, Da Silva D, et al. European guidelines for quality assurance in cervical cancer screening: recommendations for clinical management of abnormal cervical cytology, part 1. Cytopathology. 2008;19(6):342–54.CrossRef Jordan J, Arbyn M, Martin-Hirsch P, Schenck U, Baldauf JJ, Da Silva D, et al. European guidelines for quality assurance in cervical cancer screening: recommendations for clinical management of abnormal cervical cytology, part 1. Cytopathology. 2008;19(6):342–54.CrossRef
10.
go back to reference Landy R, Mathews C, Robertson M, Wiggins CL, McDonald YJ, Goldberg DW, et al. A state-wide population-based evaluation of cervical cancers arising during opportunistic screening in the United States. Gynecol Oncol. 2020;159(2):344–53.CrossRef Landy R, Mathews C, Robertson M, Wiggins CL, McDonald YJ, Goldberg DW, et al. A state-wide population-based evaluation of cervical cancers arising during opportunistic screening in the United States. Gynecol Oncol. 2020;159(2):344–53.CrossRef
11.
go back to reference Spence AR, Goggin P, Franco EL. Process of care failures in invasive cervical cancer: systematic review and meta-analysis. Prev Med. 2007;45(2):93–106.CrossRef Spence AR, Goggin P, Franco EL. Process of care failures in invasive cervical cancer: systematic review and meta-analysis. Prev Med. 2007;45(2):93–106.CrossRef
12.
go back to reference Murphy J, Varela NP, Elit L, Lytwyn A, Yudin M, Shier M, et al. The organization of colposcopy services in Ontario: recommended framework. Curr Oncol. 2015;22(4):287–96.CrossRef Murphy J, Varela NP, Elit L, Lytwyn A, Yudin M, Shier M, et al. The organization of colposcopy services in Ontario: recommended framework. Curr Oncol. 2015;22(4):287–96.CrossRef
13.
go back to reference Campari C, Fedato C, Iossa A, Petrelli A, Zorzi M, Anghinoni E, et al. Cervical cancer screening in immigrant women in Italy: a survey on participation, cytology and histology results. Eur J Cancer Prev. 2016;25(4):321–8.CrossRef Campari C, Fedato C, Iossa A, Petrelli A, Zorzi M, Anghinoni E, et al. Cervical cancer screening in immigrant women in Italy: a survey on participation, cytology and histology results. Eur J Cancer Prev. 2016;25(4):321–8.CrossRef
14.
go back to reference Carrillo T, Montealegre JR, Bracamontes CG, Scheurer ME, Follen M, Mulla ZD. Predictors of timely diagnostic follow-up after an abnormal Pap test among Hispanic women seeking care in El Paso, Texas. BMC Womens Health. 2021;21(1):11.CrossRef Carrillo T, Montealegre JR, Bracamontes CG, Scheurer ME, Follen M, Mulla ZD. Predictors of timely diagnostic follow-up after an abnormal Pap test among Hispanic women seeking care in El Paso, Texas. BMC Womens Health. 2021;21(1):11.CrossRef
15.
go back to reference Collier R, Quinlivan JA. Domestic violence is a leading risk factor in default from colposcopy services. J Obstet Gynaecol Res. 2014;40(6):1785–90.CrossRef Collier R, Quinlivan JA. Domestic violence is a leading risk factor in default from colposcopy services. J Obstet Gynaecol Res. 2014;40(6):1785–90.CrossRef
16.
go back to reference Douglas E, Wardle J, Massat NJ, Waller J. Colposcopy attendance and deprivation: a retrospective analysis of 27,193 women in the NHS Cervical Screening Programme. Br J Cancer. 2015;113(1):119–22.CrossRef Douglas E, Wardle J, Massat NJ, Waller J. Colposcopy attendance and deprivation: a retrospective analysis of 27,193 women in the NHS Cervical Screening Programme. Br J Cancer. 2015;113(1):119–22.CrossRef
17.
go back to reference Elit L, Krzyzanowska M, Saskin R, Barbera L, Razzaq A, Lofters A, et al. Sociodemographic factors associated with cervical cancer screening and follow-up of abnormal results. Can Fam Physician. 2012;58(1):e22-31.PubMedPubMedCentral Elit L, Krzyzanowska M, Saskin R, Barbera L, Razzaq A, Lofters A, et al. Sociodemographic factors associated with cervical cancer screening and follow-up of abnormal results. Can Fam Physician. 2012;58(1):e22-31.PubMedPubMedCentral
18.
go back to reference Green LI, Mathews CS, Waller J, Kitchener H, Rebolj M, Committee THPS. Attendance at early recall and colposcopy in routine cervical screening with human papillomavirus testing. Int J Cancer. 2021;148(8):1850–7.CrossRef Green LI, Mathews CS, Waller J, Kitchener H, Rebolj M, Committee THPS. Attendance at early recall and colposcopy in routine cervical screening with human papillomavirus testing. Int J Cancer. 2021;148(8):1850–7.CrossRef
19.
go back to reference Miller SM, Tagai EK, Wen KY, Lee M, Hui SA, Kurtz D, et al. Predictors of adherence to follow-up recommendations after an abnormal Pap smear among underserved inner-city women. Patient Educ Couns. 2017;100(7):1353–9.CrossRef Miller SM, Tagai EK, Wen KY, Lee M, Hui SA, Kurtz D, et al. Predictors of adherence to follow-up recommendations after an abnormal Pap smear among underserved inner-city women. Patient Educ Couns. 2017;100(7):1353–9.CrossRef
20.
go back to reference Ogilvie GS, Shaw EA, Lusk SP, Zazulak J, Kaczorowski JA. Access to colposcopy services for high-risk Canadian women: can we do better? Can J Public Health. 2004;95(5):346–51.CrossRef Ogilvie GS, Shaw EA, Lusk SP, Zazulak J, Kaczorowski JA. Access to colposcopy services for high-risk Canadian women: can we do better? Can J Public Health. 2004;95(5):346–51.CrossRef
21.
go back to reference Sharp L, Cotton S, Thornton A, Gray N, Cruickshank M, Whynes D, et al. Who defaults from colposcopy? A multi-centre, population-based, prospective cohort study of predictors of non-attendance for follow-up among women with low-grade abnormal cervical cytology. Eur J Obstet Gynecol Reprod Biol. 2012;165(2):318–25.CrossRef Sharp L, Cotton S, Thornton A, Gray N, Cruickshank M, Whynes D, et al. Who defaults from colposcopy? A multi-centre, population-based, prospective cohort study of predictors of non-attendance for follow-up among women with low-grade abnormal cervical cytology. Eur J Obstet Gynecol Reprod Biol. 2012;165(2):318–25.CrossRef
22.
go back to reference Fish LJ, Moorman PG, Wordlaw-Stintson L, Vidal A, Smith JS, Hoyo C. Factors associated with adherence to follow-up colposcopy. Am J Health Educ. 2013;44(6):293–8.CrossRef Fish LJ, Moorman PG, Wordlaw-Stintson L, Vidal A, Smith JS, Hoyo C. Factors associated with adherence to follow-up colposcopy. Am J Health Educ. 2013;44(6):293–8.CrossRef
23.
go back to reference Eggleston KS, Coker AL, Das IP, Cordray ST, Luchok KJ. Understanding barriers for adherence to follow-up care for abnormal pap tests. J Womens Health. 2007;16(3):311–30.CrossRef Eggleston KS, Coker AL, Das IP, Cordray ST, Luchok KJ. Understanding barriers for adherence to follow-up care for abnormal pap tests. J Womens Health. 2007;16(3):311–30.CrossRef
24.
go back to reference Buick C, Murphy KJ, Howell D, Metcalfe K. Understanding the role of oncogenic human papillomavirus (HPV) status on adherence behaviors among women with abnormal cervical cytology. BMC Womens Health. 2021;21(1):29.CrossRef Buick C, Murphy KJ, Howell D, Metcalfe K. Understanding the role of oncogenic human papillomavirus (HPV) status on adherence behaviors among women with abnormal cervical cytology. BMC Womens Health. 2021;21(1):29.CrossRef
25.
go back to reference Swancutt DR, Greenfield SM, Luesley DM, Wilson S. Women’s experience of colposcopy: a qualitative investigation. BMC Womens Health. 2011;11:11.CrossRef Swancutt DR, Greenfield SM, Luesley DM, Wilson S. Women’s experience of colposcopy: a qualitative investigation. BMC Womens Health. 2011;11:11.CrossRef
26.
go back to reference Young A, Cotton S, Cruickshank ME. Information needs of young women vaccinated against HPV attending colposcopy: a qualitative study. BMC Womens Health. 2018;18(1):200.CrossRef Young A, Cotton S, Cruickshank ME. Information needs of young women vaccinated against HPV attending colposcopy: a qualitative study. BMC Womens Health. 2018;18(1):200.CrossRef
27.
go back to reference Liang LA, Einzmann T, Franzen A, Schwarzer K, Schauberger G, Schriefer D, et al. Cervical cancer screening: comparison of conventional Pap smear test, liquid-based cytology, and human papillomavirus testing as stand-alone or cotesting strategies. Cancer Epidemiol Biomark Prev. 2021;30(3):474–84.CrossRef Liang LA, Einzmann T, Franzen A, Schwarzer K, Schauberger G, Schriefer D, et al. Cervical cancer screening: comparison of conventional Pap smear test, liquid-based cytology, and human papillomavirus testing as stand-alone or cotesting strategies. Cancer Epidemiol Biomark Prev. 2021;30(3):474–84.CrossRef
28.
go back to reference Radde K, Gottschalk A, Bussas U, Schülein S, Schriefer D, Seifert U, et al. Invitation to cervical cancer screening does increase participation in Germany: results from the MARZY study. Int J Cancer. 2016;139(5):1018–30.CrossRef Radde K, Gottschalk A, Bussas U, Schülein S, Schriefer D, Seifert U, et al. Invitation to cervical cancer screening does increase participation in Germany: results from the MARZY study. Int J Cancer. 2016;139(5):1018–30.CrossRef
30.
go back to reference Bennetts A, Irwig L, Oldenburg B, Simpson JM, Mock P, Boyes A, et al. PEAPS-Q: a questionnaire to measure the psychosocial effects of having an abnormal pap smear. Psychosocial effects of abnormal Pap smears questionnaire. J Clin Epidemiol. 1995;48(10):1235–43.CrossRef Bennetts A, Irwig L, Oldenburg B, Simpson JM, Mock P, Boyes A, et al. PEAPS-Q: a questionnaire to measure the psychosocial effects of having an abnormal pap smear. Psychosocial effects of abnormal Pap smears questionnaire. J Clin Epidemiol. 1995;48(10):1235–43.CrossRef
31.
go back to reference Shinn E, Basen-Engquist K, Le T, Hansis-Diarte A, Bostic DS, Martinez-Cross J, et al. Distress after an abnormal Pap smear result: scale development and psychometric validation. Prev Med. 2004;39(2):404–12.CrossRef Shinn E, Basen-Engquist K, Le T, Hansis-Diarte A, Bostic DS, Martinez-Cross J, et al. Distress after an abnormal Pap smear result: scale development and psychometric validation. Prev Med. 2004;39(2):404–12.CrossRef
33.
go back to reference Rebolj M, Lynge E. Incomplete follow-up of positive HPV tests: overview of randomised controlled trials on primary cervical screening. Br J Cancer. 2010;103(3):310–4.CrossRef Rebolj M, Lynge E. Incomplete follow-up of positive HPV tests: overview of randomised controlled trials on primary cervical screening. Br J Cancer. 2010;103(3):310–4.CrossRef
34.
go back to reference Benard VB, Lawson HW, Eheman CR, Anderson C, Helsel W. Adherence to guidelines for follow-up of low-grade cytologic abnormalities among medically underserved women. Obstet Gynecol. 2005;105(6):1323–8.CrossRef Benard VB, Lawson HW, Eheman CR, Anderson C, Helsel W. Adherence to guidelines for follow-up of low-grade cytologic abnormalities among medically underserved women. Obstet Gynecol. 2005;105(6):1323–8.CrossRef
35.
go back to reference Beckmann MW, Quaas J, Bischofberger A, Kämmerle A, Lux MP, Wesselmann S. Establishment of the certification system “gynaecological dysplasia” in Germany. Geburtshilfe Frauenheilkd. 2014;74(9):860–7.CrossRef Beckmann MW, Quaas J, Bischofberger A, Kämmerle A, Lux MP, Wesselmann S. Establishment of the certification system “gynaecological dysplasia” in Germany. Geburtshilfe Frauenheilkd. 2014;74(9):860–7.CrossRef
36.
go back to reference Wordlaw-Stinson L, Jones S, Little S, Fish L, Vidal A, Smith JS, et al. Challenges and recommendations to recruiting women who do not adhere to follow-up gynecological care. Open J Prev Med. 2014;4(3):123–8.CrossRef Wordlaw-Stinson L, Jones S, Little S, Fish L, Vidal A, Smith JS, et al. Challenges and recommendations to recruiting women who do not adhere to follow-up gynecological care. Open J Prev Med. 2014;4(3):123–8.CrossRef
37.
go back to reference McBride E, Marlow LAV, Forster AS, Ridout D, Kitchener H, Patnick J, et al. Anxiety and distress following receipt of results from routine HPV primary testing in cervical screening: the psychological impact of primary screening (PIPS) study. Int J Cancer. 2020;146:2113–21.CrossRef McBride E, Marlow LAV, Forster AS, Ridout D, Kitchener H, Patnick J, et al. Anxiety and distress following receipt of results from routine HPV primary testing in cervical screening: the psychological impact of primary screening (PIPS) study. Int J Cancer. 2020;146:2113–21.CrossRef
38.
go back to reference de Bie R, Massuger L, Lenselink C, Derksen Y, Prins J, Bekkers R. The role of individually targeted information to reduce anxiety before colposcopy: a randomised controlled trial. BJOG. 2011;118(8):945–50.CrossRef de Bie R, Massuger L, Lenselink C, Derksen Y, Prins J, Bekkers R. The role of individually targeted information to reduce anxiety before colposcopy: a randomised controlled trial. BJOG. 2011;118(8):945–50.CrossRef
39.
go back to reference O’Connor M, O’Leary E, Waller J, Gallagher P, Martin CM, O’Leary JJ, et al. Socio-economic variations in anticipated adverse reactions to testing HPV positive: implications for the introduction of primary HPV-based cervical screening. Prev Med. 2018;115:90–6.CrossRef O’Connor M, O’Leary E, Waller J, Gallagher P, Martin CM, O’Leary JJ, et al. Socio-economic variations in anticipated adverse reactions to testing HPV positive: implications for the introduction of primary HPV-based cervical screening. Prev Med. 2018;115:90–6.CrossRef
40.
go back to reference Arbyn M, Smith SB, Temin S, Sultana F, Castle P. Detecting cervical precancer and reaching underscreened women by using HPV testing on self samples: updated meta-analyses. BMJ. 2018;363: k4823.CrossRef Arbyn M, Smith SB, Temin S, Sultana F, Castle P. Detecting cervical precancer and reaching underscreened women by using HPV testing on self samples: updated meta-analyses. BMJ. 2018;363: k4823.CrossRef
Metadata
Title
Colposcopy non-attendance following an abnormal cervical cancer screening result: a prospective population-based cohort study
Authors
Linda A. Liang
Sylke R. Zeissig
Gunther Schauberger
Sophie Merzweiler
Kathrin Radde
Sabine Fischbeck
Hans Ikenberg
Maria Blettner
Stefanie J. Klug
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Women's Health / Issue 1/2022
Electronic ISSN: 1472-6874
DOI
https://doi.org/10.1186/s12905-022-01851-6

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