|
 
 |
| REVIEW ARTICLE |
|
| Year : 2023 | Volume
: 13
| Issue : 2 | Page : 74-80 |
|
Human papillomavirus self-sampling for cervical cancer screening: Review on the acceptance, accuracy, feasibility and incorporation in the National Screening Programme of India
Amey Oak1, K Sivaranjini2, Ruchi Pathak2, Rajesh Dikshit2
1 Division of Hospital Based Cancer Registry and Patterns of Cancer Care, Centre for Cancer Epidemiology, Tata Memorial Centre, Mumbai, Maharashtra, India
2 Centre for Cancer Epidemiology, Tata Memorial Centre, Mumbai, Maharashtra, India
| Date of Submission | 11-Jan-2023 |
| Date of Decision | 03-Feb-2023 |
| Date of Acceptance | 16-Mar-2023 |
| Date of Web Publication | 28-Apr-2023 |
Correspondence Address:
Dr. Amey Oak
B-101, Nikhil Heights, Sajjan Wadi, Mithaghar Road, Mulund East, Mumbai, Maharashtra
India
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/cmrp.cmrp_12_23
Screening along with treatment is the foremost tool for cervical cancer elimination in addition to vaccination strategies. At present, India lacks a comprehensive screening programme. There are huge issues in terms of feasibility, acceptability and implementation of the existing cervical screening programme in the country. Less than 2% (Urban-2.2% and Rural-1.7%) of women in India have been screened. The current strategy recommended by Ministry of Health and Family Welfare is Visual Inspection with Acetic Acid (VIA) every 5 years for women aged between 30 and 65 years. A significant improvement in terms of decreasing incidence and mortality of cervical cancer has been seen in two randomized controlled trials conducted in India. However, VIA lacks sensitivity, requires extensive training to be given to the medical staff for accurate diagnosis, has substantial operator variability and has less acceptability among women when compared to the newer methods of cervical cancer screening such as human papillomavirus (HPV) self-sampling. HPV self-sampling is a more sensitive, accurate and more acceptable method of cervical cancer screening for women in India and abroad. It can help the existing VIA-based strategy of cervical screening by increasing participation resulting in more population being screened in the various geographical regions and populations in India. However, VIA-based screening should also be continued because of its affordability and cost-effectiveness in India where there is a significant population belonging to low socio-economic background. There are numerous evidences such as systematic reviews, meta-analyses, randomised controlled trials of India and abroad that have been used as sources in this review article to come to the conclusion that HPV self-sampling is an acceptable, accurate and sensitive method that can be used as a primary screening tool in cervical cancer screening programmes globally and in India. It can also be used as an effective triage test for prioritising high-risk populations who require urgent and effective treatment for cervical pre-cancer and cancer. To conclude, HPV self-sampling should be integrated and implemented by the government and private sector in addition to VIA-based screening strategies for achieving the goal of cervical cancer elimination in India.
Keywords: Cancer screening, cervical cancer, human papillomavirus self-sampling, India
How to cite this article:
Oak A, Sivaranjini K, Pathak R, Dikshit R. Human papillomavirus self-sampling for cervical cancer screening: Review on the acceptance, accuracy, feasibility and incorporation in the National Screening Programme of India. Curr Med Res Pract 2023;13:74-80 |
How to cite this URL:
Oak A, Sivaranjini K, Pathak R, Dikshit R. Human papillomavirus self-sampling for cervical cancer screening: Review on the acceptance, accuracy, feasibility and incorporation in the National Screening Programme of India. Curr Med Res Pract [serial online] 2023 [cited 2023 May 30];13:74-80. Available from: http://www.cmrpjournal.org/text.asp?2023/13/2/74/375229 |
| Introduction | |  |
Cervical cancer is the fourth most prevalent and often diagnosed cancer in women with an estimated 604,127 (3.1%) new cancer cases and 341,831 (3.3%) deaths globally in the year 2020.[1] India alone contributes to slightly less than one-fourth of global incidence and mortality of cervical cancer.[2] Persistent infection with oncogenic human papillomavirus (HPV) contributes to more than 95% of cervical cancers.
The World Health Organisation (WHO) has recommended that women should be screened for cervical cancer at least twice in their lifetime with a high-performance test. There are challenges to the implementation of this recommendation, but we need to address them to ensure maximum participation of the eligible population for screening.
Screening along with the treatment is one of the foremost tool for eliminating cervical cancer in addition to vaccination and other health promotion strategies. However, as of right now, India lacks a comprehensive screening programme. According to the National Family Health Survey-5 data, hardly 1.9% (Urban: 2.2% and Rural: 1.7%) of women in India had been screened for cervical cancer.[3] Ministry of Health and Family Welfare recommends carrying out a Visual Inspection with Acetic Acid (VIA) every 5 years for women aged between 30 and 65 years.[4] A significant decline in the incidence (hazard ratio 0.75 [95% confidence interval 0.55–0.95]) and mortality (0.65 [0.47–0.89]) of cervical cancer following VIA screening was observed in two randomised controlled trial (RCT) trials[5],[6] conducted in India. However, VIA lacks sensitivity and has substantial operator variability, especially when older women have endocervical lesions, and it needs resources for high-intensity quality.[7] The major hurdles to cervical cancer screening uptake in low- and middle-income countries (LMICs) include insufficient knowledge and understanding, embracement, time constraints and lack of support networks, according to a systematic study by Devarapalli et al.[8] The aforesaid challenges are addressed by HPV self-sampling since it empowers women to execute their own testing and has the extra value of preserving human resources.
The causal relationship between persistent oncogenic HPV infection and cervical cancer is presently supported by the epidemiological research.[9],[10] Nearly all invasive cervical cancer specimens and the great majority (>95%) of early cervical cancer precursors include HPV DNA.[11],[12],[13] HPV 16 and 18 variants infected almost 70% of precancerous cervical lesions. cytology/VIA-based screening may be superseded by the molecular test-based direct detection of HPV in cervical specimens. The HPV cannot be grown in the culture and detection of the virus relies on a variety of techniques. The two assays most widely used for the detection of HPV are polymerase chain reaction (PCR) with generic primers and the hybrid capture 2 (HC2) assay.
The HC2 method has been clinically verified to detect 13 high-risk HPV strains and has excellent clinical sensitivity. The test results are interpreted objectively and without the inherent subjectivity of cervical cytology or visual screening techniques. In addition to detecting women with cervical cancer, HPV DNA testing also identifies those at risk for developing cervical intraepithelial neoplasia (CIN) over the succeeding 3–10 years. This is essential for developing nations like India which may not have sufficient resources to screen all eligible women every 5–10 years but have sufficient funds to screen high-risk women who have tested positive for HPV DNA at more periodic intervals. The main advantage of the HPV-DNA molecular test is the feasibility of self-collection.[14] This review article tried to assess the acceptability and feasibility of HPV DNA self-sampling at the end-user level.
| Acceptability of Human Papillomavirus Self Sampling | | |
Self-sampling reduces the economic and logistical burden for the patient and gives an initial sense of privacy and independence.
In India, in a recent study in rural villages of Mysore district in South India, about concordance and acceptability of self-versus clinician sampling for HPV testing, it was found that self-sampling was rated remarkably higher than clinician sampling in all measures of acceptability.[15] Furthermore, in a recent study of HPV self-sampling among Indian women in Mumbai by Tata Memorial Hospital, the overall acceptance of HPV self-sampling was 97% in the target population. It was found that the acceptance of self-sampling was 100% in health education arm and 94% in the education arm. Primary awareness for cervical cancer including steps demonstrating the method to collect the self-sample was explained in the local language using flip charts and posters by medical social workers in the health education arm. The pamphlet arm had participants who were given pamphlets by medical social workers containing self-explanatory pictorial illustrations demonstrating the steps of the procedure of collecting the HPV self-sample. The findings of this study reinforce the acceptability of HPV self-sampling as a primary screening test in the targeted population.[16]
A recent meta-analysis of 37 studies among 18,516 women from 24 countries indicate that there is a strong acceptance of HPV self-sampling and a preference for self-sampling over clinician sampling.[17] In two large studies in Netherlands, each among over 25,000 women who had not responded to invitations for visit to clinic and Pap test, one-third of the women returned a self-sampling device when provided with the option.[18],[19] In a study in Norway, offering 3000 women with an invite for self-sampling instead of physician sampling visit led to increase in attendance to 33.4 from 23.2%.[20] In a similar study in Sweden among 4060 women who were not screened in at least 6 years, 39% accepted the invite for self-sampling and HPV testing, but only 9% accepted an invitation for a Pap smear.[21] A study in London demonstrated that sending self-sampling kits to persistent non-responders resulted in a 2.27-fold increase in participation rate in the screening programme as compared to when invitations were sent out to attend for cervical cytology.[22] Participation rates among 8000 women in a study in Australia were much higher when self-sampling was offered (20.3%) as compared to when Pap smear reminder was sent (6.0%).[23] A greater difference was seen in a study of 7650 women in Argentina, in which 86% women responded to an offer of self-sampling as compared to 20% women who responded to invites from an health clinic, representing a fourfold increase in patient compliance.[24]
A systematic review of different interventions to increase patient screening for various types of cancer combined seven European studies on screening for cervical cancer indicates that mailing a device for HPV self-sampling to the patient directly resulted in a 2.37-fold higher participation of population in non-responders when compared with a reminder for Pap smear testing in a clinic.[25] A recent meta-analysis of 10 studies from Europe and North America showed that the compliance of HPV self-sampling among women was 2.14 times higher as compared to when an invitation was sent for Pap smear.[26]
A positive experience was recorded among women participating in self-sampling trials for screening of cervical cancer. In a Hong Kong trial of self-sampling before undergoing a Pap smear, versus undergoing Pap smear first, most women opted for self-sampling. It was seen that introducing self-sampling increased participation rates among women for screening by 6.5%.[27] A study among 1069 women in Mexico reported that Pap test caused more pain, discomfort and embarrassment than self-sampling.[28]
It can be concluded from all the above evidences that HPV self-sampling significantly improves the participation of women in screening and there is a greater acceptability of HPV self-sampling when compared to other methods of screening for cervical cancer like Pap smear and HPV co-testing among women.
| Comparison with Clinician-Collected Samples for Human Papillomavirus Detection | | |
Patients and physicians have raised concerns about whether self-sampling is comparable to cervical clinician sampling for hrHPV (high-risk HPV) detection. Meta-analyses and systematic reviews between 2005 and 2007 have shown the results of moderate to good HPV positivity agreement (Kappa coefficient ranging from 0.24 to 0.96, overall sensitivity of 0.74 and specificity of 0.88) between these two sampling methods.[29],[30],[31] Recent studies have shown an excellent performance of self-collected specimens for HPV infection diagnosis. A meta-analysis in 2014 by Arbyn et al. analysing the data from 36 studies (on a total of 154,556 women) was used to evaluate the sensitivity, diagnostic accuracy of HPV detection on vaginal self-samples versus cervical clinician collected samples to detect lesions which were CIN2 or worse (CIN 2+).[32] The sensitivity for HPV detection by self-sampling was no different than clinician sampling for detecting CIN3+. Self-sampling when compared to cytology, using LSIL as a threshold, showed that self-sampling was 14% more sensitive to detect CIN2+. The above results show that self-sampling is a comparable and excellent option for women who do not participate in screening programmes which involve physician sampling.[32] In India, in the study of concordance and acceptability of self-versus clinician sampling for HPV testing in rural villages of Mysore district in South India, the self-sampled vaginal swabs when compared to the clinician sampling for HPV DNA testing had a greater specificity (98.1%) than sensitivity (66.7%). The overall concordance between the two tests was 94.1%. There have been several studies comparing HPV screening results from self-collected and clinician-collected specimens in LMICs with all demonstrating high levels of agreement.[15] Comparison of self-collected samples and clinician-collected cervical samples from 5318 women in Scotland showed results that self-sampling and clinician sampling are equally sensitive and specific in detecting precancerous stages of the cervix.[33] In another study in Netherlands, including 2049 women, showed 96.8% hrHPV prevalence concordance between cervico-vaginal samples taken by self-collection and physician taken cervical smears.[34] These studies provide a robust support for the HPV detection on self-obtained specimens, with results comparable to clinician-collected cervical samples.[35]
| HPV Self Sampling with a Follow Up Pap Test is More Sensitive Than a Pap Test Alone | | |
HPV self-sampling with a Pap smear on follow-up, to address a positive HPV result has proven to be more sensitive than a Pap smear alone. The conclusion form a meta-analysis by Snijders et al. was that that hrHPV testing is at least as, if not more sensitive for CIN2+ as histology on clinician-obtained specimens.[36] The detection of hrHPV using self-sampling has shown less specificity when compared to clinician-collected samples, but the increased sensitivity of self-sampling and HPV testing versus clinician-obtained Pap smear could potentially decrease the mortality and morbidity associated with cervical cancer.[37] Other studies have also shown similar results that HPV testing from self-collected samples is highly sensitive. For example, in a group of 615 women in Costa Rica, HPV testing was found to be more sensitive for detecting CIN2+ than cytology. In addition, this study also showed that the proportion of women with initial normal baseline cytology that can develop to CIN2+ during follow-up is three times higher than the proportion of women with HPV negative results (obtained from self-collection) that can develop CIN2+ later.[25] This suggests that HPV screening may be more informative than cytology for predicting future cancer related abnormalities. In a study performed among 2000 Swedish women, women were sent invites for either self-sampling in combination with an HPV test, or a Pap smear by a clinician. Women who were found to be HPV positive were subsequently invited for further examination and biopsy. The odds ratio of finding histological CIN2 or CIN3 lesions with self-sampling in comparison to Pap smear was 5.4.[21] Self sampling can also be used for HPV screening to detect more HPV affected individuals in the population. In an Italian study among 700 women, it was found that the chance of a woman having a positive cytology score was 10 times higher in the case of a self-sampled positive hrHPV result.[38] In another study in France among 20,000 women, showed that CIN 2 + detection was higher among women who were offered self-sampling versus women who were invited for a Pap smear.[39]
The evidences from these studies show that the use of self-sampling in detecting HPV with a follow up Pap smear is a useful aid for the detecting abnormal cytologies and better in terms of detection when compared with Pap smear.
| Human Papillomavirus Self Sampling in Covid Era and Beyond | | |
The COVID-19 pandemic has had a significant impact on cervical cancer screening. There was postponement of public screening initiatives and programmes in 2020 and disruption in cancer treatment services due to the cancellation of planned visits, decreased availability of public transport, lack of staff, shortage of medicines and diagnostic services.[40]
There were also surprising opportunities for expanding cervical cancer screening strategies and programmes in terms of an expanded diagnostic molecular testing infrastructure, supply chains and overall increase in molecular testing activity. The accessibility and availability of excellent infrastructure and highly trained personnel were allocated for working on HPV molecular testing.[41],[42],[43]
HPV self-sampling is now a popular method of screening during and post-pandemic to get to never or under-screened populations.[44],[45] It has become a feasible strategy for mid and post-pandemic catch-up screening. A recent study from Tata Memorial Hospital showed that among women residing in urban slums, non-urban slums and women from rural settings, acceptance rate for self-sampling was 99.2%, 97% and 98.8% and HPV positivity was 7%, 7.8% and 7.8%, respectively.[16] In their response to WHO's 2020 call for the elimination of cervical cancer as a public health priority, a European task force incorporated self-sampling into organised screening programmes to aid for achieving the WHO goal in Europe.[46] In a current study in the USA, 72.7% of women reported high readiness and inclination to use an HPV self-sampling kit at home,[47] findings are similar in other studies in the USA.[48],[49],[50],[51],[52],[53],[54],[55] In the first RCT to evaluate the feasibility of mailing self-sampling kits to underscreened women in the USA, more than half the women chose to return a self-collected sample as an alternative to in-office screening.[56] In the rural population of Ontario, Canada, it was found that women who were overdue for screening were in all probability, 3.7 times more likely to go for screening with a self-sampling kit as those who received the standard-of-care opportunistic screening.[57] In low-resource settings, community-based self-sampling with the assistance of educated personnel should be used for implementing screening programmes.
Thus, there is increasing evidence in support of self-sampling in the pandemic and post-pandemic era. Current evidence also supports HPV self-sampling as an intervention for overcoming barriers and to reach underscreened women. The COVID era has presented an opportunity to use HPV self-sampling as a viable method to accelerate towards cervical cancer elimination.[34]
| Conclusion and the Way Forward | | |
HPV self-sampling should be used as a primary screening test, especially for unscreened population and non-responders. The acceptability, sensitivity and diagnostic accuracy of self-sampling will facilitate the implementation of self-sampling as an integral component of screening programmes for cervical cancer in India and abroad. Concordance between self-sampling and clinician sampling is adequate for screening in the community settings raising the possibility that large scale screening programmes could reduce the incidence, prevalence morbidity and mortality due to cervical cancer in India and in other countries.[14] The implementation of self-sampling should be comprehensive, appropriate to local context and should cover everything from screening to treatment. Women should be offered a choice of self-sampling as it would increase the participation and cost-effectiveness of screening. In low-resource settings, offering community-based self-sampling with educated personnel to assist with the process should be considered. The emergence of COVID-19 has presented an opportunity to accelerate progress in eradication of cervical cancer by using self-sampling as an effective tool in screening programmes for cervical cancer with consideration of appropriate incorporation of diagnostics, follow-up and treatment. Effective implementation of self-sampling would help in bringing about health equity in terms of access to screening and it should be primary tool that should be used while formulating and implementing strategies to reduce the incidence and prevalence of cervical cancer in both high- and low-income settings, as well as local communities.[34] Many countries such as Netherlands, Finland and Australia have already implemented HPV self-sampling in their national cervical screening strategies, which has resulted inbetter outcomes and increased participation of their populations.[58],[59],[60],[61],[62] Other countries such as UK,[63] Switzerland,[64] Norway and Denmark[65] have initiated trials with self-sampling to evaluate incorporation of this method in their official national cervical screening programs. In addition, trials have also started which have incorporated self-sampling in certain populations with low participation such as the Maori in New Zealand,[66] Haitian, Hispanic and African-American women in South Florida,[67] women from low socio-economic background in North Carolina, USA.[68] HPV self-sampling should be implemented as a primary tool of screening in addition to VIA-based strategies, in view of its acceptability and cost-effectiveness to implement among women in all populations and geographical regions of India. The study done by Tata Memorial Centre demonstrated the acceptability of HPV self-sampling as a primary screening test, especially in resource-constraint settings and among under screened populations.[16] To conclude, integration and effective implementation of HPV self-sampling in the NPCDCS programme would have a strong and far-reaching impact on building a sustainable and operational cervical screening model for the country.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;71:209-49.  |
| 2. | India State-Level Disease Burden Initiative Cancer Collaborators. The burden of cancers and their variations across the states of India: The Global Burden of Disease Study 1990-2016. Lancet Oncol 2018;19:1289-306. |
| 3. | International Institute for Population Sciences (IIPS) and ICF. National Family Health Survey (NFHS-5), India, 2019-21: Mizoram. Mumbai: IIPS 2021. |
| 4. | Arbyn M, Sankaranarayanan R, Muwonge R, Keita N, Dolo A, Mbalawa CG, et al. Pooled analysis of the accuracy of five cervical cancer screening tests assessed in eleven studies in Africa and India. Int J Cancer 2008;123:153-60. |
| 5. | Sankaranarayanan R, Esmy PO, Rajkumar R, Muwonge R, Swaminathan R, Shanthakumari S, et al. Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: A cluster-randomised trial. Lancet 2007;370:398-406. |
| 6. | Shastri SS, Mittra I, Mishra GA, Gupta S, Dikshit R, Singh S, et al. Effect of VIA screening by primary health workers: Randomized controlled study in Mumbai, India. J Natl Cancer Inst 2014;106:dju009. |
| 7. | Silkensen SL, Schiffman M, Sahasrabuddhe V, Flanigan JS. Is it time to move beyond visual inspection with acetic acid for cervical cancer screening? Glob Health Sci Pract 2018;6:242-6. |
| 8. | Devarapalli P, Labani S, Nagarjuna N, Panchal P, Asthana S. Barriers affecting uptake of cervical cancer screening in low and middle income countries: A systematic review. Indian J Cancer 2018;55:318-26. [ PUBMED] [Full text] |
| 9. | Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-9. |
| 10. | Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003;348:518-27. |
| 11. | Clifford GM, Smith JS, Aguado T, Franceschi S. Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: A meta-analysis. Br J Cancer 2003;89:101-5. |
| 12. | Bosch FX, Lorincz A, Muñoz N, Meijer CJ, Shah KV. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002;55:244-65. |
| 13. | de Sanjose S. Human Papillomavirus and Cancer – Epidemiology and Prevention, 4 th Monograph of the Spanish Society of Epidemiology. Barcelona, Spain: Spanish Society of Epidemiology; 2006. p. 143-7. |
| 14. | Bhatla N, Moda N. The clinical utility of HPV DNA testing in cervical cancer screening strategies. Indian J Med Res 2009;130:261-5. [ PUBMED] [Full text] |
| 15. | Madhivanan P, Nishimura H, Ravi K, Pope B, Coudray M, Arun A, et al. Acceptability and concordance of self- versus clinician- sampling for HPV testing among rural south Indian women. Asian Pac J Cancer Prev 2021;22:971-6. |
| 16. | Anand KV, Mishra GA, Pimple SA, Biswas SK, Kulkarni VY, Salunke G. Cross-Sectional Study of HPV Self-Sampling among Indian Women—A Way Forward. Indian J Med Paediatr Oncol 2022;43:103-8. |
| 17. | Nelson EJ, Maynard BR, Loux T, Fatla J, Gordon R, Arnold LD. The acceptability of self-sampled screening for HPV DNA: A systematic review and meta-analysis. Sex Transm Infect 2017;93:56-61. |
| 18. | Gök M, Heideman DA, van Kemenade FJ, Berkhof J, Rozendaal L, Spruyt JW, et al. HPV testing on self collected cervicovaginal lavage specimens as screening method for women who do not attend cervical screening: Cohort study. BMJ 2010;340:c1040. |
| 19. | Gök M, van Kemenade FJ, Heideman DA, Berkhof J, Rozendaal L, Spruyt JW, et al. Experience with high-risk human papillomavirus testing on vaginal brush-based self-samples of non-attendees of the cervical screening program. Int J Cancer 2012;130:1128-35. |
| 20. | Enerly E, Bonde J, Schee K, Pedersen H, Lönnberg S, Nygård M. Self-sampling for human papillomavirus testing among non-attenders increases attendance to the Norwegian cervical cancer screening programme. PLoS One 2016;11:e0151978. |
| 21. | Wikström I, Lindell M, Sanner K, Wilander E. Self-sampling and HPV testing or ordinary Pap-smear in women not regularly attending screening: A randomised study. Br J Cancer 2011;105:337-9. |
| 22. | Szarewski A, Cadman L, Mesher D, Austin J, Ashdown-Barr L, Edwards R, et al. HPV self-sampling as an alternative strategy in non-attenders for cervical screening – A randomised controlled trial. Br J Cancer 2011;104:915-20. |
| 23. | Sultana F, English DR, Simpson JA, Drennan KT, Mullins R, Brotherton JM, et al. Home-based HPV self-sampling improves participation by never-screened and under-screened women: Results from a large randomized trial (iPap) in Australia. Int J Cancer 2016;139:281-90. |
| 24. | Arrossi S, Thouyaret L, Herrero R, Campanera A, Magdaleno A, Cuberli M, et al. Effect of self-collection of HPV DNA offered by community health workers at home visits on uptake of screening for cervical cancer (the EMA study): A population-based cluster-randomised trial. Lancet Glob Health 2015;3:e85-94. |
| 25. | Camilloni L, Ferroni E, Cendales BJ, Pezzarossi A, Furnari G, Borgia P, et al. Methods to increase participation in organised screening programs: A systematic review. BMC Public Health 2013;13:464. |
| 26. | Racey CS, Withrow DR, Gesink D. Self-collected HPV testing improves participation in cervical cancer screening: A systematic review and meta-analysis. Can J Public Health 2013;104:e159-66. |
| 27. | Wong EL, Chan PK, Chor JS, Cheung AW, Huang F, Wong SY. Evaluation of the impact of human papillomavirus DNA self-sampling on the uptake of cervical cancer screening. Cancer Nurs 2016;39:E1-11. |
| 28. | Dzuba IG, Díaz EY, Allen B, Leonard YF, Lazcano Ponce EC, Shah KV, et al. The acceptability of self-collected samples for HPV testing vs. the pap test as alternatives in cervical cancer screening. J Womens Health Gend Based Med 2002;11:265-75. |
| 29. | Ogilvie GS, Patrick DM, Schulzer M, Sellors JW, Petric M, Chambers K, et al. Diagnostic accuracy of self collected vaginal specimens for human papillomavirus compared to clinician collected human papillomavirus specimens: A meta-analysis. Sex Transm Infect 2005;81:207-12. |
| 30. | Petignat P, Faltin DL, Bruchim I, Tramèr MR, Franco EL, Coutlée F. Are self-collected samples comparable to physician-collected cervical specimens for human papillomavirus DNA testing? A systematic review and meta-analysis. Gynecol Oncol 2007;105:530-5. |
| 31. | Stewart DE, Gagliardi A, Johnston M, Howlett R, Barata P, Lewis N, et al. Self-collected samples for testing of oncogenic human papillomavirus: A systematic review. J Obstet Gynaecol Can 2007;29:817-28. |
| 32. | Arbyn M, Verdoodt F, Snijders PJ, Verhoef VM, Suonio E, Dillner L, et al. Accuracy of human papillomavirus testing on self-collected versus clinician-collected samples: A meta-analysis. Lancet Oncol 2014;15:172-83. |
| 33. | Stanczuk G, Baxter G, Currie H, Lawrence J, Cuschieri K, Wilson A, et al. Clinical validation of hrHPV testing on vaginal and urine self-samples in primary cervical screening (cross-sectional results from the Papillomavirus Dumfries and Galloway-PaVDaG study). BMJ Open 2016;6:e010660. |
| 34. | Ketelaars PJ, Bosgraaf RP, Siebers AG, Massuger LF, van der Linden JC, Wauters CA, et al. High-risk human papillomavirus detection in self-sampling compared to physician-taken smear in a responder population of the Dutch cervical screening: Results of the VERA study. Prev Med 2017;101:96-101. |
| 35. | Gupta S, Palmer C, Bik EM, Cardenas JP, Nuñez H, Kraal L, et al. Self-sampling for human papillomavirus testing: Increased cervical cancer screening participation and incorporation in international screening programs. Front Public Health 2018;6:77. |
| 36. | Snijders PJ, Verhoef VM, Arbyn M, Ogilvie G, Minozzi S, Banzi R, et al. High-risk HPV testing on self-sampled versus clinician-collected specimens: A review on the clinical accuracy and impact on population attendance in cervical cancer screening. Int J Cancer 2013;132:2223-36. |
| 37. | Porras C, Hildesheim A, González P, Schiffman M, Rodríguez AC, Wacholder S, et al. Performance of self-collected cervical samples in screening for future precancer using human papillomavirus DNA testing. J Natl Cancer Inst 2015;107:400. |
| 38. | Igidbashian S, Boveri S, Radice D, Casadio C, Spolti N, Sandri MT, et al. Performance of self-sampled HPV test in comparison with liquid based cytology. Eur J Obstet Gynecol Reprod Biol 2014;177:72-6. |
| 39. | Sancho-Garnier H, Tamalet C, Halfon P, Leandri FX, Le Retraite L, Djoufelkit K, et al. HPV self-sampling or the Pap-smear: A randomized study among cervical screening nonattenders from lower socioeconomic groups in France. Int J Cancer 2013;133:2681-7. |
| 40. | WHO NCD Department. Final Results Rapid Assessment of Service Delivery for Noncommunicable Disease during the COVID-19 Pandemic. Geneva, Switzerland: WHO; 2020. |
| 41. | Thompson D, Lei Y. Mini review: Recent progress in RT-LAMP enabled COVID-19 detection. Sens Actuators Rep 2020;2:100017. |
| 42. | Gao J, Wu L, Yang D, Gong W, Wang J. A one-pot CRISPR/Cas9-typing PCR for DNA detection and genotyping. J Mol Diagn 2021;23:46-60. |
| 43. | Ramachandran A, Huyke DA, Sharma E, Sahoo MK, Huang C, Banaei N, et al. Electric field-driven microfluidics for rapid CRISPR-based diagnostics and its application to detection of SARS-CoV-2. Proc Natl Acad Sci U S A 2020;117:29518-25. |
| 44. | Vaccarella S, Lortet-Tieulent J, Plummer M, Franceschi S, Bray F. Worldwide trends in cervical cancer incidence: Impact of screening against changes in disease risk factors. Eur J Cancer 2013;49:3262-73. |
| 45. | IARC. IARC Handbooks of Cancer Prevention Cervix Cancer Screening. Lyon, France: IARC; 2005. |
| 46. | Arbyn M, Gultekin M, Morice P, Nieminen P, Cruickshank M, Poortmans P, et al. The European response to the WHO call to eliminate cervical cancer as a public health problem. Int J Cancer 2021;148:277-84. |
| 47. | Bishop E, Katz ML, Reiter PL. Acceptability of human papillomavirus self-sampling among a national sample of women in the United States. Biores Open Access 2019;8:65-73. |
| 48. | Madzima TR, Vahabi M, Lofters A. Emerging role of HPV self-sampling in cervical cancer screening for hard-to-reach women: Focused literature review. Can Fam Physician 2017;63:597-601. |
| 49. | Scarinci IC, Litton AG, Garcés-Palacio IC, Partridge EE, Castle PE. Acceptability and usability of self-collected sampling for HPV testing among African-American women living in the Mississippi Delta. Womens Health Issues 2013;23:e123-30. |
| 50. | Vanderpool RC, Jones MG, Stradtman LR, Smith JS, Crosby RA. Self-collecting a cervico-vaginal specimen for cervical cancer screening: An exploratory study of acceptability among medically underserved women in rural Appalachia. Gynecol Oncol 2014;132 Suppl 1:S21-5. |
| 51. | Reiter PL, Richardson M, Zimmermann JB, Moore D, Martin KM, et al. Acceptability of Human Papillomavirus Self-Test Devices among Women from High-Risk Populations. J Women's Health, Issues Care 2016;5:1. doi:10.4172/2325-9795.1000216. |
| 52. | Richman AR, Brewer NT, Liebman AK, Rinas AC, Smith JS. Optimizing human papillomavirus self-testing for high-risk women. Sex Transm Infect 2011;87:118-22. |
| 53. | Katz ML, Zimmermann BJ, Moore D, Paskett ED, Reiter PL. Perspectives from health care providers and women about completing human papillomavirus (HPV) self testing at home. Women Health 2017; 57:1161-77. |
| 54. | Reiter PL, McRee AL. Cervical cancer screening (Pap testing) behaviours and acceptability of human papillomavirus self-testing among lesbian and bisexual women aged 21-26 years in the USA. J Fam Plann Reprod Health Care 2015;41:259-64. |
| 55. | Winer RL, Lin J, Tiro JA, Miglioretti DL, Beatty T, Gao H, et al. Effect of mailed human papillomavirus test kits vs. usual care reminders on cervical cancer screening uptake, precancer detection, and treatment: A randomized clinical trial. JAMA Netw Open 2019;2:e1914729. |
| 56. | Racey CS, Gesink DC, Burchell AN, Trivers S, Wong T, Rebbapragada A. Randomized intervention of self-collected sampling for human papillomavirus testing in under-screened rural women: Uptake of screening and acceptability. J Womens Health (Larchmt) 2016;25:489-97. |
| 57. | Lozar T, Nagvekar R, Rohrer C, Dube Mandishora RS, Ivanus U, Fitzpatrick MB. Cervical cancer screening postpandemic: Self-sampling opportunities to accelerate the elimination of cervical cancer. Int J Womens Health 2021;13:841-59. |
| 58. | Rozemeijer K, de Kok IM, Naber SK, van Kemenade FJ, Penning C, van Rosmalen J, et al. Offering self-sampling to non-attendees of organized primary HPV screening: When do harms outweigh the benefits? Cancer Epidemiol Biomarkers Prev 2015;24:773-82. |
| 59. | |
| 60. | Smith M, Lew JB, Simms K, Canfell K. Impact of HPV sample self-collection for underscreened women in the renewed Cervical Screening Program. Med J Aust 2016;204:e1941-7. |
| 61. | Karjalainen L, Anttila A, Nieminen P, Luostarinen T, Virtanen A. Self-sampling in cervical cancer screening: Comparison of a brush-based and a lavage-based cervicovaginal self-sampling device. BMC Cancer 2016;16:221. |
| 62. | Virtanen A, Anttila A, Luostarinen T, Malila N, Nieminen P. Improving cervical cancer screening attendance in Finland. Int J Cancer 2015;136:E677-84. |
| 63. | Lim AW, Hollingworth A, Kalwij S, Curran G, Sasieni P. Offering self-sampling to cervical screening non-attenders in primary care. J Med Screen 2017;24:43-9. |
| 64. | Viviano M, Catarino R, Jeannot E, Boulvain M, Malinverno MU, Vassilakos P, et al. Self-sampling to improve cervical cancer screening coverage in Switzerland: A randomised controlled trial. Br J Cancer 2017;116:1382-8. |
| 65. | Tranberg M, Bech BH, Blaakær J, Jensen JS, Svanholm H, Andersen B. Study protocol of the CHOiCE trial: A three-armed, randomized, controlled trial of home-based HPV self-sampling for non-participants in an organized cervical cancer screening program. BMC Cancer 2016;16:835. |
| 66. | Smith MA, Edwards S, Canfell K. Impact of the National Cervical Screening Programme in New Zealand by age: Analysis of cervical cancer trends 1985-2013 in all women and in Māori women. Cancer Causes Control 2017;28:1393-404. |
| 67. | Kobetz E, Seay J, Amofah A, Pierre L, Bispo JB, Trevil D, et al. Mailed HPV self-sampling for cervical cancer screening among underserved minority women: Study protocol for a randomized controlled trial. Trials 2017;18:19. |
| 68. | Anderson C, Breithaupt L, Des Marais A, Rastas C, Richman A, Barclay L, et al. Acceptability and ease of use of mailed HPV self-collection among infrequently screened women in North Carolina. Sex Transm Infect 2018;94:131-7. |
|
Search Pubmed for