Next Article in Journal
PRISM (Pictorial Representation of Illness and Self-Measure) as Visual Tool to Support Oral Health Education Prior to Endoprosthetic Joint Replacement—A Novel Approach in Dentistry
Previous Article in Journal
Assessment of Rib Fracture in Acute Trauma Using Automatic Rib Segmentation and a Curved, Unfolded View of the Ribs: Is There a Saving of Time?
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
JCM
Volume 11
Issue 9
10.3390/jcm11092503
jcm-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Acceptability of Human Papilloma Virus Self-Sampling for Cervical Cancer Screening in a Cohort of Patients from Romania (Stage 2)

by
Mihaela Grigore
1,
Ingrid-Andrada Vasilache
1,*,
Petru Cianga
2,
Daniela Constantinescu
2,
Odetta Duma
3,
Roxana Daniela Matasariu
1 and
Ioana-Sadiye Scripcariu
1
1
Department of Obstetrics and Gynecology, ‘Grigore T. Popa’ University of Medicine and Pharmacy, 700115 Iasi, Romania
2
Department of Immunology, ‘Grigore T. Popa’ University of Medicine and Pharmacy, 700115 Iasi, Romania
3
Department of Epidemiology, ‘Grigore T. Popa’ University of Medicine and Pharmacy, 700115 Iasi, Romania
*
Author to whom correspondence should be addressed.
J. Clin. Med. 2022, 11(9), 2503; https://doi.org/10.3390/jcm11092503
Submission received: 8 April 2022 / Revised: 22 April 2022 / Accepted: 28 April 2022 / Published: 29 April 2022
(This article belongs to the Section Obstetrics & Gynecology)
Versions Notes

Abstract

:
(1) Background: Low patient’s adherence to conventional cervical cancer screening methods determined the need to take into consideration alternative approaches, and vaginal HPV self-sampling is one of them. We aimed to evaluate, using an online survey, the Romanian women’s acceptability of vaginal HPV self-sampling. (2) Methods: A 13-questions online survey was distributed on three Facebook groups, and the results were summarized. (3) Results: Despite of good educational background, 10.8% (n = 60) of the respondents did not know what a Pap smear is, and 33% (n = 183) were not informed about the free national cervical cancer screening program. Multivariate analysis revealed an increased likelihood of vaginal self-sampling acceptance among respondents who did not know about Pap test (OR: 7.80; 95%CI: 1.062–57.431; p = 0.021), national cervical cancer screening program (OR: 1.96; 95%CI: 1.010–3.806; p = 0.02), HPV infection (OR: 7.35; 95%CI: 3.099–17.449; p< 0.001) or HPV test (OR: 1.67; 95%CI: 0.950–2.948; p = 0.03). Moreover, women who did not previously undergo a cervical cancer screening program were more likely to accept the new screening method (OR: 1.62; 95%CI: 0.878–3.015; p = 0.04). (4) Conclusions: Our results showed high acceptability rates of vaginal HPV self-sampling among participants.

1. Introduction

With an estimated 604,000 new cases and 342,000 deaths worldwide in 2020, cervical cancer is the fourth most commonly diagnosed cancer and the fourth major cause of cancer death in women [1]. Each year in Romania approximately 1800 women die from cervical cancer, and almost 3400 receive this diagnosis [2,3]. The high incidence and mortality rates associated with cervical cancer place this country in the top of the European Union statistics [4].
Human papillomavirus (HPV) infection, some sexually transmittable infections (HIV and Chlamydia trachomatis), smoking, high parity, and long-term use of oral contraceptives are among the risk factors for developing cervical cancer [5,6]. HPV oncogenic types 16 and 18, responsible for almost 70% of the cervical neoplasia cases [7], are the main target of public health strategies for eradicating cervical cancer.
Because of the highly efficient primary (HPV vaccine) and secondary (screening) prevention strategies, cervical cancer is regarded as a preventable disease. However, low patients’ adherence to the national screening programs, mainly due to the lack of information and understanding, represented a barrier for achieving consistent results [8].
In recent years, vaginal HPV self-sampling emerged as a promising alternative to the conventional screening strategies based on Pap smears and/or HPV DNA testing. HPV self-sampling is a screening procedure that involves using a kit to collect cervico-vaginal samples, which are then sent to a laboratory for genotyping high-risk oncogenic HPV strains. It is easy to use by patients at home, is cost-effective, and has good overall accuracy in detecting HPV strains. Although recent studies have indicated that provider-collected cervical samples had the highest HPV-DNA sensitivity (84–100%), self-collected vaginal HPV-DNA tests appeared to have good performance, with a sensitivity ranging from 66 to 88% [9,10,11]. If the patient receives a positive result for the HPV test, she will establish an appointment with the gynecologist for deciding the best therapeutic plan.
Furthermore, self-sampling was found to be superior to HPV DNA testing performed by a clinician in terms of acceptance and preference [12,13]. The main benefits cited for vaginal self-sampling were less pain or physical discomfort, convenience, ability to perform the test in private, and less embarrassment or anxiety [14,15,16,17,18].
The challenges associated with the implementation of vaginal self-sampling include: difficulties regarding explaining the self-sampling procedure to participating women, specimen transportation and laboratory processing, as well as follow-up of positive women [19]. The provision of clear instructions accompanied by illustrations in suitable language would be a feasible approach for facilitating the self-sampling procedure [20,21].
On the other hand, the SARS-CoV-2 pandemic has accelerated the introduction of HPV self-sampling as a measure to increase the addressability to cervical cancer screening program, and self-sampling is included in the World Health Organization’s (WHO) recently issued guidelines on self-intervention for health, as well as the cervical cancer screening guidelines [22]. A recent study assessed the effectiveness of HPV self-sampling for cervical cancer screening during the SARS-CoV-2 pandemic, and found a high concordance for HPV detection between self-sampled and clinician-sampled specimens (90.2%), as well as a high willingness to repeat the procedure under the same conditions (89.2% of the participants) [23].
The main determinant of this study was the lack of literature data on the acceptability of doing self-sampling in the local population. We aimed to evaluate, using an online survey, the Romanian women’s acceptability of vaginal HPV self-sampling.

2. Materials and Methods

Between 15 February and 16 March 2022, data were collected using a Qualtrics form prepared by the investigator and titled: ‘A survey for analyzing the Romanian women’s thoughts regarding vaginal HPV self-sampling’, which was posted on three Facebook groups (Mothers at first pregnancy, About kids, and Mothers from Iasi).
The survey consisted of 13 questions that addressed maternal characteristics (age, living environment, and level of education), cervical cancer screening topic (6 closed questions that evaluated the women’s knowledge and experience with cervical cancer screening), as well as the women’s acceptability of vaginal HPV self-sampling. The participants were also shown an illustration of a vaginal self-sampling device along with its instructions for use so that they could complete the questionnaire fully informed.
The questionnaire was posted once group administrators approved it, and participants were notified that their anonymous responses would be published in this study. Before beginning the survey, all participants were instructed that it was completely voluntary and anonymous, and that they could skip any questions they did not feel comfortable answering or exit at any time. Each participant was instructed to read and declare if she agreed or disagreed with the survey’s questions. No names or medical identifying numbers were recorded to safeguard the participants’ privacy. All procedures were followed in compliance with the applicable norms and legislation. The Institutional Ethics Committee of the University of Medicine and Pharmacy ‘Grigore T. Popa’ gave its approval to this investigation (No. 96/23.06.2021).
Data collected were translated from the Romanian language into standard English. Incomplete surveys were excluded from the study. The total number of questionnaires distributed allowed statistical analysis with a cut-off for the absolute error and the type one error of 5%.
Acceptability of vaginal self-sampling was defined as the target variable. Categorical parameters were expressed as numbers and percentages, and statistical comparisons were made using the Chi-square test. We used a multivariate logistic regressions analysis to explore the associations between demographic characteristics, knowledge about the cervical cancer screening, previous screening attendance, and the target variable. The statistical analysis was performed using SPSS software (version 28.0.1, IBM Corporation, Armonk, NY, USA). A p value of less than 0.05 was considered statistically significant.

3. Results

Five hundred and eighty-two questionnaires were obtained and analyzed. Only 556 were included in the study due to incomplete data. Table 1 and Table 2 describe the acceptability of vaginal self-sampling for cervical screening among our respondents.
The majority of the respondents belonged to the 30–40 years age group (n = 339; 60.9%%), and only a minority of respondents had more than 51 years (n = 28; 5%). Most participants lived in urban areas (n = 324; 58.2%), and had a bachelor degree (n = 264; 47.4%).
Despite of good educational background, 10.9% (n = 61) of the respondents did not know what a Pap smear was, and 33% (n = 184) were not informed about the free national cervical cancer screening program. The results from the univariate analysis showed a significant association between age, medium, level of education, and the acceptability of vaginal HPV self-sampling (p < 0.001).
The odds ratios (OR) and 95% confidence intervals (CI) from the multivariate logistic analysis are shown in Table 3. The women from the 20–30 years age group were the most likely to accept the new method of cervical cancer screening (OR: 15.78; 95% CI: 2.161–115.304; p = 0.003). There was also a good likelihood for accepting this screening method for women included in the 40–50 years age group (OR: 3.34; 95% CI: 1.020–10.960; p = 0.02).
Women living in rural areas (OR: 2.87; 95% CI: 1.483–5.563; p < 0.001), as well as those who possessed a high-school diploma (OR: 2.73; 95% CI: 1.478–5.057; p < 0.001), were more likely to accept the screening method. On the other hand, it appeared that respondents from urban areas (OR: 0.34; 95% CI: 0.180–0.674; p < 0.001), as well as those with a bachelor degree (OR: 0.28; 95% CI: 0.155–0.532; p < 0.001), were less likely to embrace the method.
An alarming number of respondents did not know what an HPV infection (n = 238; 42.8%) or HPV test (n = 267; 48%) was. Moreover, more than one third of the participants (n = 198; 35.6%) did not do a Pap test or an HPV test for cervical cancer screening during their lifetime. On the other hand, more than half of the women (n = 358; 64.3%) underwent cervical screening, and Pap smear was the most used screening method (n = 291; 81.2%).
Univariate analysis indicated a significant association between knowledge about Pap test (p = 0.006), national cervical screening program (p = 0.043), HPV infection (p < 0.001), previous participation to the screening program (p < 0.001) and the acceptability of vaginal HPV self-sampling.
Multivariate analysis revealed an increased likelihood of vaginal self-sampling acceptance among respondents who did not know about Pap test (OR: 7.80; 95%CI: 1.062–57.431; p = 0.021), national cervical cancer screening program (OR: 1.96; 95%CI: 1.010–3.806; p = 0.02), HPV infection (OR: 7.35; 95%CI: 3.099–17.449; p < 0.001) or HPV test (OR: 1.67; 95%CI: 0.950–2.948; p = 0.03). Moreover, women who did not previously undergo a cervical cancer screening program were more likely to accept the new screening method (OR: 1.62; 95%CI: 0.878–3.015; p = 0.04).
The majority of the respondents (n = 523; 94%) considered self-sampling a good alternative to Pap test for women who do not consult their physicians. However, 87% (n = 484) of the subjects agreed that cervical sampling performed by a doctor is better than vaginal self-sampling (p = 0.02).
64.7% (n = 360) of the participants agreed with the statement that most women will choose self-sampling over a visit to a doctor, while 81.6% of them considered HPV vaginal self-sampling a good alternative to the conventional screening method. The answers to the last two questions indicated the women’s preference of self-sampling over the doctors’ appointments, with a significant level of acceptability among the participants (p < 0.001).

4. Discussion

This observational retrospective study, based on a self-administered online survey, showed high acceptability rates of vaginal HPV self-sampling among participants, including under-screened women. Moreover, our study also confirmed the women’s lack of knowledge about cervical cancer screening, even though the majority of the respondents had higher education.
In terms of acceptability, our multivariate analysis revealed that the women from the 20–30 years age group, followed by those in the 40–50 years age group, were most likely to accept the new method of cervical cancer screening, while those women in the 30–40 years age group were significantly less likely to embrace the method (OR: 0.07; 95%CI: 0.023–0.241; p < 0.001). These findings could be explained by the fact that very young women are more open to new technologies, while those middle-aged, who are less used to regular gynecological appointments, are in favor of self-sampling in the comfort of their own home. Similar results were reported in various studies that outlined increased acceptability of vaginal self-sampling among younger generations of women due to decreased embarrassment, time/effort investment and a ‘do-it- yourself’ attitude, as well as older women, due to previous bad gynecological experiences or the need for privacy [10,24,25,26].
Our results also indicated that women living in rural areas, as well as those who possessed a high-school diploma, were more likely to accept the screening method, while those from urban areas and with a bachelor degree were less likely to accept it. Several studies demonstrated that women living in rural areas do not benefit as much as women from urban areas in terms of cervical cancer screening [27,28]. Limited accessibility to Pap smear and/or HPV testing, rural practice configuration or scarce financial resources were cited as factors that negatively influence the women’s addressability to cervical cancer screening programs [29,30]. On the other hand, developed sanitary infrastructure along with higher consumption of healthcare services in the urban areas could be considered reasons for the women’s preference to traditional cervical cancer screening [31,32]. Although the literature data are conflicting regarding the influence of the educational background over the HPV self-sampling acceptability [33,34,35], we hypothesize that women with at least a bachelor degree tend to have a higher compliance to conventional cervical cancer screening.
In Romania, there is an active national cervical cancer screening program developed by the Public Health Ministry in partnership with regional hospitals that offers free Pap testing for women aged between 25 and 64 years [36]. The lack of knowledge among the participants about the cervical cancer screening in Romania was a key finding of the study. An alarming number of respondents did not know what a Pap smear (n = 60; 10.8%), HPV infection (n = 237; 42.7%) or HPV test (n = 267; 48.1%) was despite a good educational background. These data are comparable to that outlined by various studies in developing or underdeveloped countries [37,38,39,40].
Our multivariate analysis revealed an increased likelihood of vaginal self-sampling acceptance among respondents who did not know about Pap tests, the national cervical cancer screening program, or HPV infection. Moreover, women who did not previously undergo a cervical cancer screening program appeared more likely to accept the new screening method. Our results are in line with those reported in an observational study by Lancrajan et al., which outlined the limited knowledge of Romanian women about cervical cancer screening [41]. Furthermore, previous studies indicated that self-sampling acceptability was higher among women who had never undergone cervical screening before, in both rich and underprivileged societies [42,43].
We hypothesize that women with scarce information regarding this topic would feel more comfortable with a self-administered test that does not require a visit to the gynecologist. This emphasizes the importance of a thorough education about the feasibility, benefits, and accuracy of self-sampling in order to increase screening participation.
In this study, vaginal self-sampling was considered a good alternative to Pap test for women who do not consult their physicians, with an acceptance rate of 89.7%. The main reasons for low addressability to the cervical cancer screening program in Romania were explored by Todor et al., and included the lack of national coverage and the penetration in the rural areas, mass-media promotion campaigns, funding, involvement of general practitioners, and bureaucracy, as well as program monitoring [44]. Our results showed that 33% (n = 183) of the respondents were not informed about the free national cervical cancer screening program. The present study confirmed the low adherence of Romanian respondents to the cervical cancer screening program, despite the high acceptability rates of HPV self-sampling among respondents.
Although the majority of respondents considered that cervical sampling performed by a doctor is better than vaginal self-sampling (86.9%), they have also expressed their preference to self-sampling over the doctors’ appointments (81.5% vs. 15.6%). Analysis of the patient’s preferences over these methods was not the purpose of this study, but the comfort, privacy, ergonomics, and accessibility of self-sampling were cited as some of the main reasons for choosing this alternative over a physician’s appointment [42,45,46,47].
A recent systematic review by Devarapalli et al., which evaluated the most important barriers associated with cervical cancer screening in low and middle-income countries, concluded that the following elements are important obstacles to fulfilling the screening’s objectives: psychological, structural, sociocultural, and religious barriers, as well as lack of knowledge and awareness [48]. All these aspects must be considered when establishing public health programs in order to improve the campaigns’ outcomes.
Several studies have shown that women’s awareness of cervical cancer, HPV, and its vaccine can effectively improve the mortality rates and reduce incidences of this disease [49,50,51]. Therefore, effective measures to improve women’s level of knowledge should include all new means of information (mass-media, social media platforms, news websites, etc.) that allow dissemination of relevant data on a regular basis. Moreover, telemedicine has been shown to be a useful tool for providing medical advice during the SARS-CoV-2 pandemic, and could be further added to the screening programs [52,53].
The participants’ profile, which may not be representative of under-screened women targeted by vaginal self-sampling, is one main weakness in our study. The majority of the subjects had a high educational level and a high rate of cervical cancer screening compliance. This could be explained by the way women who had access to social media platforms were recruited. We were not able to generalize the findings of this study since our participants were limited to respondents attending social media groups. Other limitations of our study include: small number of participants included, short time-frame for data collection, and restricted information concerning the epidemiological characteristics of the respondents. We chose to design this survey with only a limited number of questions that allowed a reasonable completion rate, and a 3 min response time. Similar studies, that used web-based surveys disseminated through Facebook groups, acknowledged the difficulties regarding the maintenance of an active interest for the survey and representativeness of epidemiological data [54,55].
Further research is needed to evaluate the acceptability of vaginal HPV self-sampling in various cohorts of patients, especially those who manifest low compliance to conventional screening methods.

5. Conclusions

This study demonstrated high acceptability rates of vaginal HPV self-sampling among respondents, indicating this as a feasible method for increasing the women’s compliance to cervical cancer screening.
However, an alarming number of women did not have knowledge about cervical cancer and its screening possibilities. Therefore, more education and public health interventions are needed to raise awareness about this topic.
Future studies could further evaluate the values and preferences of Romanian women regarding the secondary prevention of cervical cancer.

Author Contributions

Conceptualization, M.G., I.-S.S. and I.-A.V.; methodology, M.G., I.-S.S. and I.-A.V.; validation, P.C., D.C. and O.D.; formal analysis, M.G. and R.D.M.; investigation, I.-S.S. and I.-A.V.; data curation, P.C., D.C. and O.D.; writing—original draft preparation, M.G., I.-S.S. and I.-A.V.; writing—review and editing, M.G. and I.-A.V.; supervision, M.G.; project administration, M.G.; funding acquisition, M.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the University of Medicine and Pharmacy ‘Grigore T. Popa’, Iasi, Romania (grant IDEI No. 10309/29.06.2020).

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Institutional Ethics Committee of University of Medicine and Pharmacy ‘Grigore T. Popa’ (No. 96/23.06.2021).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to local policies.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef] [PubMed]
  2. International Agency for Research on Cancer. Globocan 2018: Romania. Available online: https://gco.iarc.fr/today/data/factsheets/populations/642-romania-fact-sheets.pdf (accessed on 15 March 2022).
  3. Arbyn, M.; Weiderpass, E.; Bruni, L.; de Sanjosé, S.; Saraiya, M.; Ferlay, J.; Bray, F. Estimates of incidence and mortality of cervical cancer in 2018: A worldwide analysis. Lancet Glob. Health 2020, 8, e191–e203. [Google Scholar] [CrossRef] [Green Version]
  4. Arbyn, M.; Raifu, A.O.; Weiderpass, E.; Bray, F.; Anttila, A. Trends of cervical cancer mortality in the member states of the European Union. Eur. J. Cancer 2009, 45, 2640–2648. [Google Scholar] [CrossRef]
  5. Human papillomaviruses. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans; International Agency for Research on Cancer: Lyon, France, 2007; Volume 90, pp. 1–636.
  6. Thun, M.; Linet, M.S.; Cerhan, J.R.; Haiman, C.A.; Schottenfeld, D. Cancer Epidemiology and Prevention; Oxford University Press: Oxford, UK, 2017. [Google Scholar]
  7. Whitlock, E.P.; Vesco, K.K.; Eder, M.; Lin, J.S.; Senger, C.A.; Burda, B.U. Liquid-Based Cytology and Human Papillomavirus Testing to Screen for Cervical Cancer: A Systematic Review for the U.S. Preventive Services Task Force. Ann. Intern. Med. 2011, 155, 687–697. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  8. Buskwofie, A.; David-West, G.; Clare, C.A. A Review of Cervical Cancer: Incidence and Disparities. J. Natl. Med. Assoc. 2020, 112, 229–232. [Google Scholar] [CrossRef] [PubMed]
  9. Aranda Flores, C.E.; Gomez Gutierrez, G.; Ortiz Leon, J.M.; Cruz Rodriguez, D.; Sørbye, S.W. Self-collected versus clinician-collected cervical samples for the detection of HPV infections by 14-type DNA and 7-type mRNA tests. BMC Infect. Dis. 2021, 21, 504. [Google Scholar] [CrossRef] [PubMed]
  10. Wong, E.L.Y.; Cheung, A.W.L.; Huang, F.; Chor, J.S.Y. Can Human Papillomavirus DNA Self-sampling be an Acceptable and Reliable Option for Cervical Cancer Screening in Female Sex Workers? Cancer Nurs. 2018, 41, 45–52. [Google Scholar] [CrossRef]
  11. Inturrisi, F.; Aitken, C.A.; Melchers, W.J.; Brule, A.J.V.D.; Molijn, A.; Hinrichs, J.W.; Niesters, H.G.; Siebers, A.G.; Schuurman, R.; Heideman, D.A.; et al. Clinical performance of high-risk HPV testing on self-samples versus clinician samples in routine primary HPV screening in the Netherlands: An observational study. Lancet Reg. Health Eur. 2021, 11, 100235. [Google Scholar] [CrossRef]
  12. Huynh, J.; Howard, M.; Lytwyn, A. Self-collection for vaginal human papillomavirus testing: Systematic review of studies asking women their perceptions. J. Low. Genit. Tract. Dis. 2010, 14, 356–362. [Google Scholar] [CrossRef]
  13. Tiro, J.A.; Betts, A.C.; Kimbel, K.; Buist, D.S.; Mao, C.; Gao, H.; Shulman, L.; Malone, C.; Beatty, T.; Lin, J.; et al. Understanding Patients’ Perspectives and Information Needs Following a Positive Home Human Papillomavirus Self-Sampling Kit Result. J. Women’s Health 2019, 28, 384–392. [Google Scholar] [CrossRef]
  14. Ilangovan, K.; Kobetz, E.; Koru-Sengul, T.; Marcus, E.N.; Rodriguez, B.; Alonzo, Y.; Carrasquillo, O. Acceptability and Feasibility of Human Papilloma Virus Self-Sampling for Cervical Cancer Screening. J. Women’s Health 2016, 25, 944–951. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Kilfoyle, K.A.; Marais, A.C.D.; Ngo, M.A.; Romocki, L.; Richman, A.R.; Barclay, L.; Brewer, N.T.; Rahangdale, L.; Smith, J.S. Preference for Human Papillomavirus Self-Collection and Papanicolaou: Survey of Underscreened Women in North Carolina. J. Low. Genit. Tract Dis. 2018, 22, 302–310. [Google Scholar] [CrossRef] [PubMed]
  16. Gottschlich, A.; Rivera-Andrade, A.; Grajeda, E.; Alvarez, C.; Montano, C.M.; Meza, R. Acceptability of Human Papillomavirus Self-Sampling for Cervical Cancer Screening in an Indigenous Community in Guatemala. J. Glob. Oncol. 2017, 3, 444–454. [Google Scholar] [CrossRef] [PubMed]
  17. Crofts, V.; Flahault, E.; Tebeu, P.M.; Untiet, S.; Boulvain, M.; Vassilakos, P.; Petignat, P.; Flore, G.K.-F.G. Education efforts may contribute to wider acceptance of human papillomavirus self-sampling. Int. J. Women’s Health 2015, 7, 149–154. [Google Scholar] [CrossRef] [Green Version]
  18. Ortiz, A.P.; Alejandro, N.; Pérez, C.M.; Otero, Y.; Soto-Salgado, M.; Palefsky, J.M.; Tortolero-Luna, G.; Romaguera, J. Acceptability of cervical and anal HPV self-sampling in a sample of Hispanic women in Puerto Rico. Puerto Rico Health Sci. J. 2012, 31, 205–212. [Google Scholar]
  19. Hawkes, D.; Keung, M.H.T.; Huang, Y.; McDermott, T.L.; Romano, J.; Saville, M.; Brotherton, J.M.L. Self-Collection for Cervical Screening Programs: From Research to Reality. Cancers 2020, 12, 1053. [Google Scholar] [CrossRef]
  20. Podolak, I.; Kisia, C.; Omosa-Manyonyi, G.; Cosby, J. Using a multimethod approach to develop implementation strategies for a cervical self-sampling program in Kenya. BMC Health Serv. Res. 2017, 17, 222. [Google Scholar] [CrossRef] [Green Version]
  21. Hanley, S.J.; Fujita, H.; Yokoyama, S.; Kunisawa, S.; Tamakoshi, A.; Dong, P.; Kobayashi, N.; Watari, H.; Kudo, M.; Sakuragi, N. HPV self-sampling in Japanese women: A feasibility study in a population with limited experience of tampon use. J. Med. Screen. 2016, 23, 164–170. [Google Scholar] [CrossRef]
  22. World Health Organization (WHO). WHO Guideline on Self-Care Interventions for Health and Well-Being. Available online: https://wwwwhoint/publications-detail-redirect/9789240030909 (accessed on 17 March 2022).
  23. Ngu, S.-F.; Lau, L.S.K.; Li, J.; Wong, G.C.Y.; Cheung, A.N.Y.; Ngan, H.Y.S.; Chan, K.K.L. Human Papillomavirus Self-Sampling for Primary Cervical Cancer Screening in Under-Screened Women in Hong Kong during the COVID-19 Pandemic. Int. J. Environ. Res. Public Health 2022, 19, 2610. [Google Scholar] [CrossRef]
  24. Bosgraaf, R.P.; Ketelaars, P.J.; Verhoef, V.M.; Massuger, L.F.; Meijer, C.J.; Melchers, W.J.; Bekkers, R.L. Reasons for non-attendance to cervical screening and preferences for HPV self-sampling in Dutch women. Prev. Med. 2014, 64, 108–113. [Google Scholar] [CrossRef]
  25. Chen, S.L.; Hsieh, P.C.; Chou, C.H.; Tzeng, Y.L. Determinants of women’s likelihood of vaginal self-sampling for human papillomavirus to screen for cervical cancer in Taiwan: A cross-sectional study. BMC Women’s Health 2014, 14, 139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Fargnoli, V.; Petignat, P.; Burton-Jeangros, C. To what extent will women accept HPV self-sampling for cervical cancer screening? A qualitative study conducted in Switzerland. Int. J. Women’s Health 2015, 7, 883–888. [Google Scholar] [CrossRef] [Green Version]
  27. Di, J.; Rutherford, S.; Chu, C. Review of the Cervical Cancer Burden and Population-Based Cervical Cancer Screening in China. Asian Pac. J. Cancer Prev. 2015, 16, 7401–7407. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Sripan, P.; Chitapanarux, I.; Tharavichitkul, E.; Muangwong, P.; Pongnikorn, D.; Waisri, N.; Hanpragopsuk, C.; Maneesai, P.; Tansiri, P.; Poungsombat, M.; et al. Disparities in the change of cervical cancer mortality rate between urban and rural Chiang Mai in the era of universal health care and the Thai national screening program. Int. J. Equity Health 2021, 20, 175. [Google Scholar] [CrossRef] [PubMed]
  29. Locklar, L.R.B.; Do, D.P. Rural-urban differences in HPV testing for cervical cancer screening. J. Rural Health 2022, 38, 409–415. [Google Scholar] [CrossRef] [PubMed]
  30. Allen-Leigh, B.; Uribe-Zúñiga, P.; León-Maldonado, L.; Brown, B.J.; Lörincz, A.; Salmeron, J.; Lazcano-Ponce, E. Barriers to HPV self-sampling and cytology among low-income indigenous women in rural areas of a middle-income setting: A qualitative study. BMC Cancer 2017, 17, 734. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  31. Yeh, P.T.; E Kennedy, C.; De Vuyst, H.; Narasimhan, M. Self-sampling for human papillomavirus (HPV) testing: A systematic review and meta-analysis. BMJ Glob. Health 2019, 4, e001351. [Google Scholar] [CrossRef]
  32. Shin, M.B.; Garcia, P.J.; Saldarriaga, E.M.; Fiestas, J.L.; Ásbjörnsdóttir, K.H.; Iribarren, S.J.; Barnabas, R.V.; Gimbel, S. Cost of community-based human papillomavirus self-sampling in Peru: A micro-costing study. Lancet Reg. Health 2021, 8, 100160. [Google Scholar] [CrossRef]
  33. Morgan, K.; Azzani, M.; Khaing, S.L.; Wong, Y.-L.; Su, T.T. Acceptability of Women Self-Sampling versus Clinician-Collected Samples for HPV DNA Testing: A Systematic Review. J. Low. Genit. Tract Dis. 2019, 23, 193–199. [Google Scholar] [CrossRef]
  34. Ma’Som, M.; Bhoo-Pathy, N.; Nasir, N.H.; Bellinson, J.; Subramaniam, S.; Ma, Y.; Yap, S.-H.; Goh, P.-P.; Gravitt, P.; Woo, Y.L. Attitudes and factors affecting acceptability of self-administered cervicovaginal sampling for human papillomavirus (HPV) genotyping as an alternative to Pap testing among multiethnic Malaysian women. BMJ Open 2016, 6, e011022. [Google Scholar] [CrossRef]
  35. Eche, M.T.; Vermaak, K. Knowledge, attitude and practice of female university students regarding human papillomavirus and self-sampling in KwaZulu-Natal, South Africa: A cross-sectional survey. BMC Women’s Health 2022, 22, 58. [Google Scholar] [CrossRef] [PubMed]
  36. Romanian Public Health Ministry. Planul National de Combatere a Cancerului (The National Plan for Fighting against Cancer). Available online: https://www.ms.ro/wp-content/uploads/2022/01/Plan-National-de-Combatere-a-Cancerului.pdf (accessed on 14 March 2022).
  37. Dahiya, N.; Aggarwal, K.; Singh, M.C.; Garg, S.; Kumar, R. Knowledge, attitude, and practice regarding the screening of cervical cancer among women in New Delhi, India. Tzu Chi Med. J. 2019, 31, 240–243. [Google Scholar] [CrossRef] [PubMed]
  38. Maree, J.E.; Kampinda-Banda, M. Knowledge and Practices of Cervical Cancer and Its Prevention Among Malawian Women. J. Cancer Educ. 2020, 35, 86–92. [Google Scholar] [CrossRef] [PubMed]
  39. Niyonsenga, G.; Gishoma, D.; Sego, R.; Uwayezu, M.G.; Nikuze, B.; Fitch, M.; Igiraneza, P.C. Knowledge, utilization and barriers of cervical cancer screening among women attending selected district hospitals in Kigali-Rwanda. Can. Oncol. Nurs. J. 2021, 31, 266–274. [Google Scholar] [CrossRef]
  40. Romli, R.; Shahabudin, S.; Saddki, N.; Mokhtar, N. Cervical cancer and pap smear screening: Knowledge, attitude and practice among working women in northern state of Malaysia. Med. J. Malays. 2019, 74, 8–14. [Google Scholar]
  41. Lancrajan, I.C.; Lisencu, I.C.; Ignat, L.F.; Trisca, R.; Topor, I.D.; Coman, M.A.; Mocean, F. Evaluation of Attitudes and Knowledge on Cervical Cancer among Women from Rural and Urban Areas of Romania. J. Women’s Health 2017, 6, 5. [Google Scholar] [CrossRef] [Green Version]
  42. Piana, L.; Leandri, F.X.; Le Retraite, L.; Heid, P.; Tamalet, C.; Sancho-Garnier, H. HPV-Hr detection by home self sampling in women not compliant with pap test for cervical cancer screening. Results of a pilot programme in Bouches-du-Rhône. Bull. Cancer 2011, 98, 723–731. [Google Scholar] [CrossRef]
  43. Rosenbaum, A.; Gage, J.C.; Alfaro, K.M.; Ditzian, L.R.; Maza, M.; Scarinci, I.C.; Felix, J.C.; Castle, P.E.; Villalta, S.; Miranda, E.; et al. Acceptability of self-collected versus provider-collected sampling for HPV DNA testing among women in rural El Salvador. Int. J. Gynecol. Obstet. 2014, 126, 156–160. [Google Scholar] [CrossRef]
  44. Todor, R.D.; Bratucu, G.; Moga, M.A.; Candrea, A.N.; Marceanu, L.G.; Anastasiu, C.V. Challenges in the Prevention of Cervical Cancer in Romania. Int. J. Environ. Res. Public Health 2021, 18, 1721. [Google Scholar] [CrossRef]
  45. Bertucci, M.; Bonnet, E.; Satger, L.; Kreiche, A.; Chappert, J.-L.; Loy-Morel, S.; Segondy, M.; Daurès, J.P.; Boulle, N. Acceptability of vaginal self-sampling with high-risk human papillomavirus testing for cervical cancer screening: A French questionnaire-based study. Women Health 2021, 61, 83–94. [Google Scholar] [CrossRef]
  46. Montealegre, J.R.; Landgren, R.M.; Anderson, M.L.; Hoxhaj, S.; Williams, S.; Robinson, D.J.; Scheurer, M.E.; Ramondetta, L.M. Acceptability of self-sample human papillomavirus testing among medically underserved women visiting the emergency department. Gynecol. Oncol. 2015, 138, 317–322. [Google Scholar] [CrossRef] [PubMed]
  47. Verdoodt, F.; Jentschke, M.; Hillemanns, P.; Racey, C.; Snijders, P.; Arbyn, M. Reaching women who do not participate in the regular cervical cancer screening programme by offering self-sampling kits: A systematic review and meta-analysis of randomised trials. Eur. J. Cancer 2015, 51, 2375–2385. [Google Scholar] [CrossRef] [PubMed]
  48. Asthana, S.; Devarapalli, P.; Labani, S.; Nagarjuna, N.; Panchal, P. Barriers affecting uptake of cervical cancer screening in low and middle income countries: A systematic review. Indian J. Cancer 2018, 55, 318–326. [Google Scholar] [CrossRef] [PubMed]
  49. Strohl, A.E.; Mendoza, G.; Ghant, M.S.; Cameron, K.A.; Simon, M.A.; Schink, J.C.; Marsh, E.E. Barriers to prevention: Knowledge of HPV, cervical cancer, and HPV vaccinations among African American women. Am. J. Obstet. Gynecol. 2014, 212, 65.e1–65.e5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Wong, L.P.; Sam, I.C. Ethnically diverse female university students’ knowledge and attitudes toward human papillomavirus (HPV), HPV vaccination and cervical cancer. Eur. J. Obstet. Gynecol. Reprod. Biol. 2010, 148, 90–95. [Google Scholar] [CrossRef]
  51. Lin, W.; Wang, Y.; Liu, Z.; Chen, B.; Yuan, S.; Wu, B.; Gong, L. Awareness and attitude towards human papillomavirus and its vaccine among females with and without daughter(s) who participated in cervical cancer screening in Shenzhen, China. Trop. Med. Int. Health 2019, 24, 1054–1063. [Google Scholar] [CrossRef]
  52. Masson, H. Cervical pap smears and pandemics: The effect of COVID-19 on screening uptake & opportunities to improve. Women’s Health 2021, 17, 3–4. [Google Scholar] [CrossRef]
  53. Hincapié, M.A.; Gallego, J.C.; Gempeler, A.; Piñeros, J.A.; Nasner, D.; Escobar, M.F. Implementation and Usefulness of Telemedicine During the COVID-19 Pandemic: A Scoping Review. J. Prim. Care Community Health 2020, 11, 2150132720980612. [Google Scholar] [CrossRef]
  54. Kebede, M.M.; Schuett, C.; Pischke, C.R. The Role of Continuous Glucose Monitoring, Diabetes Smartphone Applications, and Self-Care Behavior in Glycemic Control: Results of a Multi-National Online Survey. J. Clin. Med. 2019, 8, 109. [Google Scholar] [CrossRef] [Green Version]
  55. Grow, A.; Perrotta, D.; Del Fava, E.; Cimentada, J.; Rampazzo, F.; Gil-Clavel, S.; Zagheni, E. Addressing Public Health Emergencies via Facebook Surveys: Advantages, Challenges, and Practical Considerations. J. Med. Internet Res. 2020, 22, e20653. [Google Scholar] [CrossRef]
Table
Table 1. The acceptability of vaginal HPV self-sampling among the respondents, considering the demographic characteristics and cervical cancer screening knowledge.
Table 1. The acceptability of vaginal HPV self-sampling among the respondents, considering the demographic characteristics and cervical cancer screening knowledge.
VariableSelf-Sampling Acceptance (n/%)Total Number of Responses (n/%)p Value
YesNo
Age20–30 years108 (19.4%)1 (0.1%)109 (19.6%)<0.001
30–40 years285 (51.2%)54 (9.7%)339 (69.9%)
40–50 years78 (14%)3 (0.5%)81(14.5%)
>51 years27 (4.8%)1 (0.1%)28 (5%)
MediumUrban282 (50.7%)42 (7.5%)324 (58.3%)<0.001
Rural216 (38.8%)16 (2.8%)232 (41.7%)
Level of educationPrimary school (≤4 years of study)3 (0.5%)1 (0.1%)4 (0.7%)<0.001
Pre-high school (5–8 years of study)26 (4.6%)1 (0.1%)27 (4.8%)
High-school (9–12 years of study)246 (44.2%)15 (2.6%)261 (46.9%)
≥Bachelor degree222 (39.9%)42 (7.5%)264 (47.4%)
Do you know what Pap test is?Yes438 (78.7%)57 (10.2%)495 (89%)0.006
No60 (10.7%)1 (0.1%)62 (11%)
Do you know that in Romania there is a free national program for Pap testing?Yes327 (58.8%)45 (8.1%)372 (66.9%)0.043
No171 (30.8%)13 (2.3%)184 (33.1%)
Do you know what Human papilloma virus (HPV) infection is?Yes267 (48%)51 (9.1%)318 (57.1%)<0.001
No231 (41.5%)7 (1.2%)238 (42.9%)
Do you know what HPV test is?Yes252 (45.3%)37 (6.6%)289 (51.9%)0.072
No246 (44.2%)21 (3.7%)267 (48.1%)
Did you previously do a Pap test or HPV test for cervical cancer screening?Yes315 (56.6%)43 (7.7%)358 (64.3%)<0.001
No183 (32.1%)15 (2.6%)198 (35.7%)
If your previous answer was yes, which test did you take?Pap test264 (47.4%)27 (4.8%)291 (81.2%)<0.001
HPV test3 (0.5%)1 (0.1%)4 (1.1%)
Both45 (8%)18 (3.2%)63 (17.7%)
Table
Table 2. The acceptability of vaginal HPV self-sampling among the respondents, considering their opinions regarding cervical cancer screening.
Table 2. The acceptability of vaginal HPV self-sampling among the respondents, considering their opinions regarding cervical cancer screening.
VariableSelf-Sampling Acceptance (n/%)Total Number of Responses (n/%)p Value
YesNo
Do you consider self-sampling a good alternative to Pap test for women who do not consult their physicians?Yes498 (89.5%)25 (4.4%)523 (94.1%)<0.001
No0 (0%)30 (5.4%)30 (5.4%)
I have no opinion0 (0%)3 (0.5%)3 (0.5%)
I consider that cervical sampling performed by a doctor is better than self-samplingYes430 (77.3%)54 (9.7%)484 (87%)0.02
No39 (7%)0 (0%)39 (7%)
I have no opinion30 (5.4%)3 (0.5%)33 (6%)
I consider that most women will choose self-sampling over a visit to a doctorYes339 (61%)21 (3.7%)360 (64.7%)<0.001
No109 (19.6%)27 (4.8%)136 (24.4%)
I have no opinion51 (9.1%)9 (1.6%)60 (10.7%)
I consider self-sampling a good alternative and I would use it instead of going to the doctorYes442 (79.4%)12 (2.1%)454 (81.6%)<0.001
No45 (8.1%)42 (7.5%)87 (15.6%)
I have no opinion12 (2.1%)3 (0.5%)15 (21.7%)
Table
Table 3. Multivariate logistic regression analysis to identify factors associated with the acceptability of HPV self-sampling.
Table 3. Multivariate logistic regression analysis to identify factors associated with the acceptability of HPV self-sampling.
VariableSelf-Sampling Acceptancep Value
Odds ratioLower Bound CIUpper Bound CI
Age20–30 years15.782.161 115.3040.003
30–40 years0.070.0230.241<0.001
40–50 years3.341.020 10.9600.02
>51 years3.260.43624.5030.12
MediumUrban0.340.1800.674<0.001
Rural2.871.483 5.563<0.001
Level of educationPrimary school (≤4 years of study)0.340.035 3.3760.18
Pre-high school (5–8 years of study)3.260.436 24.5030.12
High-school (9–12 years of study)2.731.4785.057<0.001
≥Bachelor degree0.280.155 0.532<0.001
Did women know about Pap test?Yes0.120.0170.9420.021
No7.801.062 57.4310.021
Did women know about the free national screening program?Yes0.500.263 0.9900.02
No1.961.010 3.8060.02
Did women know about Human papilloma virus (HPV) infection?Yes0.130.057 0.323<0.001
No7.353.099 17.449<0.001
Did women know about HPV test? Yes0.590.339 1.0530.03
No1.670.950 2.9480.03
Were women previously screened for cervical cancer?Yes0.610.332 1.1390.04
No1.620.878 3.0150.04
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Grigore, M.; Vasilache, I.-A.; Cianga, P.; Constantinescu, D.; Duma, O.; Matasariu, R.D.; Scripcariu, I.-S. Acceptability of Human Papilloma Virus Self-Sampling for Cervical Cancer Screening in a Cohort of Patients from Romania (Stage 2). J. Clin. Med. 2022, 11, 2503. https://doi.org/10.3390/jcm11092503

AMA Style

Grigore M, Vasilache I-A, Cianga P, Constantinescu D, Duma O, Matasariu RD, Scripcariu I-S. Acceptability of Human Papilloma Virus Self-Sampling for Cervical Cancer Screening in a Cohort of Patients from Romania (Stage 2). Journal of Clinical Medicine. 2022; 11(9):2503. https://doi.org/10.3390/jcm11092503

Chicago/Turabian Style

Grigore, Mihaela, Ingrid-Andrada Vasilache, Petru Cianga, Daniela Constantinescu, Odetta Duma, Roxana Daniela Matasariu, and Ioana-Sadiye Scripcariu. 2022. "Acceptability of Human Papilloma Virus Self-Sampling for Cervical Cancer Screening in a Cohort of Patients from Romania (Stage 2)" Journal of Clinical Medicine 11, no. 9: 2503. https://doi.org/10.3390/jcm11092503

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop