Barriers and Facilitators of Romanian HPV (Human Papillomavirus) Vaccination
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design, Setting, and Participants
2.2. Survey Questionnaire and Data Collection
2.3. Ethical Approval
2.4. Statistical Analysis
3. Results
4. Discussion
Limitations of the Study
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Manolescu, L.S.C.; Mitran, C.I.; Mitran, M.I.; Georgescu, S.R.; Tampa, M.; Suciu, I.; Suciu, G.; Popa, G.L.; Popa, M.I. Knowledge, attitudes and beliefs about HPV infection and HPV vaccines in Romanian medical students. Arch. Microbiol. Immunol. 2021, 80, 22–35. [Google Scholar] [CrossRef]
- Tampa, M.; Mitran, C.I.; Mitran, M.I.; Nicolae, I.; Dumitru, A.; Matei, C.; Manolescu, L.; Popa, G.L.; Caruntu, C.; Georgescu, S.R. The Role of Beta HPV Types and HPV-Associated Inflammatory Processes in Cutaneous Squamous Cell Carcinoma. J. Immunol. Res. 2020, 2020, 5701639. [Google Scholar] [CrossRef] [PubMed]
- Shapiro, G.K. HPV Vaccination: An Underused Strategy for the Prevention of Cancer. Curr. Oncol. 2022, 29, 3780–3792. [Google Scholar] [CrossRef]
- Vänskä, S.; Luostarinen, T.; Baussano, I.; Apter, D.; Eriksson, T.; Natunen, K.; Nieminen, P.; Paavonen, J.; Pimenoff, V.N.; Pukkala, E.; et al. Vaccination with Moderate Coverage Eradicates Oncogenic Human Papillomaviruses If a Gender-Neutral Strategy Is Applied. J. Infect. Dis. 2020, 222, 948–956. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lehtinen, M.; Luostarinen, T.; Vänskä, S.; Söderlund-Strand, A.; Eriksson, T.; Natunen, K.; Apter, D.; Baussano, I.; Harjula, K.; Hokkanen, M.; et al. Gender-neutral vaccination provides improved control of human papillomavirus types 18/31/33/35 through herd immunity: Results of a community randomized trial (III). Int. J. Cancer 2018, 143, 2299–2310. [Google Scholar] [CrossRef] [PubMed]
- Lehtinen, M.; Pimenoff, V.N. Moral dilemma(s) in human papillomavirus vaccination-revisiting the role of the herd effect. Eurosurveillance 2021, 26, 2101154. [Google Scholar] [CrossRef]
- Niță, I.; Nițipir, C.; Toma, S.A.; Limbău, A.M.; Pîrvu, E.; Bădărău, A.I.; Suciu, I.; Suciu, G.; Manolescu, L.S.C. Correlation between Androgen Receptor Expression and Immunohistochemistry Type as Prognostic Factors in a Cohort of Breast Cancer Patients: Result from a Single-Center, Cross Sectional Study. Healthcare 2021, 9, 277. [Google Scholar] [CrossRef] [PubMed]
- Nita, I.; Nitipir, C.; Toma, S.A.; Limbău, A.M.; Pîrvu, E.; Bădărău, I.A.; Suciu, I.; Suciu, G.; Manolescu, L.S.C. Histological Aspects and Quantitative Assessment of Ki67 as Prognostic Factors in Breast Cancer Patients: Result from a Single-Center, Cross Sectional Study. Medicina 2020, 56, 600. [Google Scholar] [CrossRef] [PubMed]
- De Martel, C.; Georges, D.; Bray, F.; Ferlay, J.; Clifford, G.M. Global burden of cancer attributable to infections in 2018: A worldwide incidence analysis. Lancet Glob. Health 2020, 8, e180–e190. [Google Scholar] [CrossRef] [Green Version]
- CDC. HPV for Healthcare Professionals. HPV: Information for Healthcare Professionals. Available online: https://www.cdc.gov/hpv (accessed on 11 September 2022).
- Bruni, L.; Saura-Lázaro, A.; Montoliu, A.; Brotons, M.; Alemany, L.; Diallo, M.S.; Afsar, O.Z.; LaMontagne, D.S.; Mosina, L.; Contreras, M.; et al. HPV vaccination introduction worldwide and WHO and UNICEF estimates of national HPV immunization coverage 2010–2019. Prev. Med. 2021, 144, 106399. [Google Scholar] [CrossRef]
- Maier, C.; Maier, T.; Neagu, C.E.; Vlădăreanu, R. Romanian adolescents’ knowledge and attitudes towards human papillomavirus infection and prophylactic vaccination. Eur. J. Obs. Gynecol. Reprod. Biol. 2015, 195, 77–82. [Google Scholar] [CrossRef] [PubMed]
- Ministry of Health Press Realese. Available online: https://www.ms.ro/2022/08/31/ (accessed on 12 September 2022).
- ICO/IARC Information Centre on HPV and Cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in Romania. Summary Report. 2019. Available online: https://hpvcentre.net/statistics/reports/XWX.pdf (accessed on 12 September 2022).
- Romania National Vaccination Schedule. Available online: https://insp.gov.ro/wp-content/uploads/2022/08/Calendar-de-vaccinare-2022.pdf (accessed on 12 September 2022).
- Popa, G.L.; Muntean, A.-A.; Muntean, M.-M.; Popa, M.I. Knowledge and Attitudes on Vaccination in Southern Romanians: A Cross-Sectional Questionnaire. Vaccines 2020, 8, 774. [Google Scholar] [CrossRef] [PubMed]
- Manolescu, L.S.C.; Zaharia, C.N.; Dumitrescu, A.I.; Prasacu, I.; Radu, M.C.; Boeru, A.C.; Boidache, L.; Nita, I.; Necsulescu, A.; Medar, C.; et al. COVID-19 Parental Vaccine Hesitancy in Romania: Nationwide Cross-Sectional Study. Vaccines 2022, 10, 493. [Google Scholar] [CrossRef]
- Manolescu, L.S.C.; Zaharia, C.N.; Dumitrescu, A.I.; Prasacu, I.; Radu, M.C.; Boeru, A.C.; Boidache, L.; Nita, I.; Necsulescu, A.; Chivu, R.D. Early COVID-19 vaccination of Romanian medical and social personnel. Vaccines 2021, 9, 1127. [Google Scholar] [CrossRef] [PubMed]
- Otelea, M.R.; Zugravu, C.; Rascu, A.; Arghir, O.C.; Manolescu, L.S.C.; Mates, D. Coronasomnia in Employees without a Direct Contact with COVID-19 Infected Patients in Their Workplace. Healthcare 2022, 10, 1194. [Google Scholar] [CrossRef]
- WHO Vaccine Position Papers/Human Papillomavirus (HPV). Available online: https://www.who.int/teams/immunization-vaccines-and-biologicals/policies/position-papers/human-papillomavirus-(hpv) (accessed on 13 September 2022).
- Sharmaa, S.J.; Schartingerc, V.H.; Wuerdemanna, N.; Langerd, C.; Möllenhoffe, K.; Collinf, L.; Suttonf, L.; Riedlh, D.; Kreuteri, A.; Lechnerg, M.; et al. Awareness of Human Papillomavirus (HPV) and HPV Vaccination amongst the General Population in Germany: Lack of Awareness and Need for Action. Oncol. Res. Treat. 2022, 45, 561–567. [Google Scholar] [CrossRef]
- Kreidl, P.; Breitwieser, M.-M.; Würzner, R.; Borena, W. 14-year-old Schoolchildren can Consent to Get Vaccinated in Tyrol, Austria: What do They know about Diseases and Vaccinations? Vaccines 2020, 8, 610. [Google Scholar] [CrossRef] [PubMed]
- Mennini, F.S.; Silenzi, A.; Marcellusi, A.; Conversano, M.; Siddu, A.; Rezza, G. HPV Vaccination during the COVID-19 Pandemic in Italy: Opportunity Loss or Incremental Cost. Vaccines 2022, 10, 1133. [Google Scholar] [CrossRef] [PubMed]
- Darraj, A.I.; Arishy, A.M.; Alshamakhi, A.H.; Osaysi, N.A.; Jaafari, S.M.; Sumayli, S.A.; Mushari, R.Y.; Alhazmi, A.H. Human Papillomavirus Knowledge and Vaccine Acceptability in Jazan Province, Saudi Arabia. Vaccines 2022, 10, 1337. [Google Scholar] [CrossRef]
- Pennella, R.A.; Ayers, K.A.; Brandt, H.M. Understanding How Adolescents Think about the HPV Vaccine. Vaccines 2020, 8, 693. [Google Scholar] [CrossRef]
- Redd, D.S.; Jensen, J.L.; Bodily, R.J.; Lee, A.A.; Skyles, T.J.; Poole, B.D. Cautious Sexual Attitudes Diminish Intent to Vaccinate Children against HPV in Utah. Vaccines 2022, 10, 1382. [Google Scholar] [CrossRef] [PubMed]
- Yagi, A.; Ueda, Y.; Nakagawa, S.; Ikeda, S.; Kakuda, M.; Hiramatsu, K.; Miyoshi, A.; Kobayashi, E.; Kimura, T.; Mizushima, T.; et al. Can Catch-Up Vaccinations Fill the Void Left by Suspension of the Governmental Recommendation of HPV Vaccine in Japan? Vaccines 2022, 10, 1455. [Google Scholar] [CrossRef] [PubMed]
- Colomé-Ceballos, L.; Clua-Espuny, J.L.; Fernández-Sáez, J.; Ceballos-García, C.; Andrés-Cubells, N.; Pla-Farnós, M.J. HPV Vaccination Coverage Rate in a Rural Area: An Observational, Retrospective, and Cohort Study. Vaccines 2022, 10, 1274. [Google Scholar] [CrossRef] [PubMed]
- Chen, G.; Wu, B.; Dai, X.; Zhang, M.; Liu, Y.; Huang, H.; Mei, K.; Wu, Z. Gender Differences in Knowledge and Attitude towards HPV and HPV Vaccine among College Students in Wenzhou, China. Vaccines 2022, 10, 10. [Google Scholar] [CrossRef] [PubMed]
- Paul, P.; Fabio, A. Literature review of HPV vaccine delivery strategies: Considerations for school- and non-school based immunization program. Vaccine 2014, 32, 320–326. [Google Scholar] [CrossRef] [PubMed]
- Sypień, P.; Zielonka, T.M. Knowledge and Awareness of Polish Parents on Vaccination against Human Papillomavirus. Vaccines 2022, 10, 1156. [Google Scholar] [CrossRef]
- Goessl, C.L.; Christianson, B.; Hanson, K.E.; Polter, E.J.; Olson, S.C.; Boyce, T.G.; Dunn, D.; Williams, C.L.; Belongia, E.A.; McLean, H.Q.; et al. Human papillomavirus vaccine beliefs and practice characteristics in rural and urban adolescent care providers. BMC Public Health 2022, 22, 1322. [Google Scholar] [CrossRef] [PubMed]
- Lin, C.; Mullen, J.; Smith, D.; Kotarba, M.; Kaplan, S.J.; Tu, P. Healthcare Providers’ Vaccine Perceptions, Hesitancy, and Recommendation to Patients: A Systematic Review. Vaccines 2021, 9, 713. [Google Scholar] [CrossRef] [PubMed]
- Dragomirescu, C.C.; Lixandru, B.E.; Coldea, I.L.; Corneli, O.N.; Pana, M.; Palade, A.M.; Cristea, V.C.; Suciu, I.; Suciu, G.; Manolescu, L.S.C.; et al. Antimicrobial Susceptibility Testing for Corynebacterium Species Isolated from Clinical Samples in Romania. Antibiotics 2020, 9, 31. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Manolescu, L.S.C.; Boeru, C.; Căruntu, C.; Dragomirescu, C.C.; Goldis, M.; Jugulete, G.; Marin, M.; Popa, G.L.; Preda, M.; Radu, M.C.; et al. Romanian experience of syphilis in pregnancy and childbirth. Midwifery 2019, 78, 58–63. [Google Scholar] [CrossRef] [PubMed]
- Dragomirescu, C.C.; Lixandru, B.E.; Coldea, I.L.; Palade, A.M.; Baltoiu, M.; Dinu, S.; Cristea, V.C.; Manolescu, L.; Popa, M.I. Comparative analysis of different phenotypic and molecular methods used for the taxonomic identification of Corynebacterium spp. isolated from clinical samples in Romania. Rom. Biotechnol. Lett. 2017, 22, 12926–12933. [Google Scholar]
- Manolescu, L.; Marinescu, P. Sex differences in HIV-1 viral load and absolute CD4 cell count in long term survivors HIV-1 infected patients from Giurgiu, Romania. Rom. Rev. Lab. Med. 2013, 21, 217–224. [Google Scholar] [CrossRef] [Green Version]
- Marinescu, P.; Manolescu, L.S.C. Association of hepatitis B infection in patients with HIV Encephalopathy. Rom. Biotechnol. Lett. 2012, 17, 7817–7824. [Google Scholar]
- Manolescu, L.; Temereanca, A.; Diaconu, C.C.; Ruta, S. Correlation between resistance profile and immunosuppression in heavily treated HIV-1 infected Romanian patients. Rom. Biotechnol. Lett. 2011, 16, 6439–6449. [Google Scholar]
- Yuen, W.; Lee, A.; Chan, P.; Tran, L.; Sayko, E. Uptake of human papillomavirus (HPV) vaccination in Hong Kong: Facilitators and barriers among adolescent girls and their parents. PLoS ONE 2018, 13, e194159. [Google Scholar] [CrossRef] [Green Version]
- Veldwijk, J.; van der Heide, I.; Rademakers, J.; Schuit, A.J.; de Wit, G.A.; Uiters, E.; Lambooij, M.S. Preferences for Vaccination: Does Health Literacy Make a Difference? Med. Decis. Making 2015, 35, 948–958. [Google Scholar] [CrossRef] [PubMed]
- Francis, M.R.; Nohynek, H.; Larson, H.; Balraj, V.; Mohan, V.R.; Kang, G.; Nuorti, J.P. Factors associated with routine childhood vaccine uptake and reasons for nonvaccination in India: 1998–2008. Vaccine 2018, 36, 6559–6566. [Google Scholar] [CrossRef] [PubMed]
- Lu, P.J.; O’Halloran, A.; Kennedy, E.D.; Williams, W.W.; Kim, D.; Fiebelkorn, A.P.; Donahue, S.; Bridges, C.B. Awareness among adults of vaccine-preventable diseases and recommended vaccinations, United States, 2015. Vaccine 2017, 35, 3104–3115. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sallam, M.; Al-Mahzoum, K.; Eid, H.; Assaf, A.M.; Abdaljaleel, M.; Al-Abbadi, M.; Mahafzah, A. Attitude towards HPV Vaccination and the Intention to Get Vaccinated among Female University Students in Health Schools in Jordan. Vaccines 2021, 9, 1432. [Google Scholar] [CrossRef]
- Kolek, C.O.; Opanga, S.A.; Okalebo, F.; Birichi, A.; Kurdi, A.; Godman, B.; Meyer, J.C. Impact of Parental Knowledge and Beliefs on HPV Vaccine Hesitancy in Kenya—Findings and Implications. Vaccines 2022, 10, 1185. [Google Scholar] [CrossRef] [PubMed]
- Bencherit, D.; Kidar, R.; Otmani, S.; Sallam, M.; Samara, K.; Barqawi, H.J.; Lounis, M. Knowledge and Awareness of Algerian Students about Cervical Cancer, HPV and HPV Vaccines: A Cross-Sectional Study. Vaccines 2022, 10, 1420. [Google Scholar] [CrossRef] [PubMed]
- Osaghae, I.; Chido-Amajuoyi, O.G.; Shete, S. Healthcare Provider Recommendations and Observed Changes in HPV Vaccination Acceptance during the COVID-19 Pandemic. Vaccines 2022, 10, 1515. [Google Scholar] [CrossRef] [PubMed]
Characteristics | N = 1122 (100%) |
---|---|
Vaccinated against HPV | 118 (10.51%) |
Intention to vaccinate against HPV | 132 (11.76%) |
Infected with HPV | 99 (8.82%) |
Gender (Women) | 999 (89.04%) |
Age (median, min-max) | 38 (19–62) |
Responders < 27 years | 282 (25.13%) |
Geographic area (Urban) | 930 (82.89%) |
Domain of activity: medical | 459 (40.91%) |
Domain of activity: student | 206 (18.36%) |
Studies | |
High School | 249 (22.19%) |
Post-secondary school | 186 (16.58%) |
University/Post-university studies | 684 (60.96%) |
Have children | 666 (59.36%) |
Have heard of HPV | 1023 (91.18%) |
Have HPV information from medic | 324 (28.88%) |
HPV vaccine poses no risk | 823 (73.35%) |
Characteristics | Did Not Vaccinate against HPV Their Child/Children | Intention to Vaccinate against HPV Their Child/Children | They Vaccinated against HPV Their Child/Children | p |
---|---|---|---|---|
Age (average ± standard deviation) | 44 ± 7 | 39.64 ± 6.9 | 43.2 ± 7 | 0.00 |
Women | 321 | 231 | 54 | 0.645 |
Studies | ||||
High School | 27 | 12 | 6 | 0.093 |
Post-secondary school | 93 | 45 | 15 | |
University/Post-university studies | 228 | 198 | 39 | |
Geographic area (Urban) | 276 | 2016 | 45 | |
Domain of activity: medical | 180 | 102 | 27 | 0.016 |
Infected with HPV | 21 | 33 | 3 | |
Have heard of HPV | 315 | 249 | 6o | |
Have HPV information from medic | 138 | 138 | 44 | |
HPV vaccine pose no risk | 207 | 222 | 52 | |
HPV vaccination mandatory | 150 | 30 | 15 | 0.00 |
High cost of HPV vaccine | 57 | 78 | 6 |
Responders who did not vaccinate versus responders who vaccinated | ORa | 95% CI | |
Man versus women | 0.218 | [0.064–0.742] | |
Highschool versus university (studies) | 0.107 | [0.026–0.444] | |
Non-medical information sources versus medical | 0.035 | [0.004–0.314] | |
Reticence because of lack of information versus reticence from other causes | 22.14 | [9–54] | |
Reticence because price versus reticence from other causes | 7.8 | [2.7–22.3] | |
Responders intended to vaccinate versus responders who vaccinated | ORa | 95% CI | |
Non-medical occupation versus medical occupation | 0.156 | [0.031–0.784] | |
Highschool versus university | 0.122 | [0.028–0.533] | |
Not infected versus infected | 0.278 | [0.074–0.99] | |
Reticence because of lack of info versus reticence from other causes | 12.22 | [4.95–30.1] | |
Reticence because of price versus reticence from other causes | 14.6 | [5.18–41.2] |
Characteristics | N = 67 |
---|---|
Infected with HPV | 18 (26.87%) |
Gender (Women) | 67 (100%) |
Age (median, min-max) | 42 (28–55) |
Geographic area (Urban) | 58 (86.57%) |
Studies | |
High School | 6 (8.96%) |
Post-secondary school | 10 (14.93%) |
University/Post-university studies | 51 (76.12%) |
Domain of activity: medical | 45 (67.16%) |
Characteristics | N = 282 |
---|---|
Infected with HPV | 21 (7.44%) |
Gender (Women) | 279 (98.94%) |
Age (median, min-max) | 22 (19–26) |
Geographic area (Urban) | 225 (79.79%) |
Vaccinated against HPV | 30 (10.64%) |
With Intention to Vaccinate against HPV | 93 (32.98%) |
Studies | |
High School | 198 (70.21%) |
Post-secondary school | 6 (2.13%) |
University/Post-university studies | 78 (27.66%) |
Domain of activity: medical | 30 (10.64%) |
Domain of activity: student | 206 (73.05%) |
B | E.S. | Wald | p | ORa | Lower CI 95% | Upper CI 95% | |
---|---|---|---|---|---|---|---|
Age | −0.242 | 0.247 | 0.959 | 0.327 | 0.785 | 0.483 | 1.275 |
Gender (woman vs. men) | −0.774 | 0.436 | 3.154 | 0.076 | 0.461 | 0.196 | 1.083 |
Studies (university and more vs. high school and secondary school) | −0.213 | 0.220 | 0.945 | 0.331 | 0.808 | 0.525 | 1.242 |
Geographic area (urban vs. rural) | −0.660 | 0.228 | 8.416 | 0.004 | 0.517 | 0.331 | 0.807 |
HPV vaccination to be included in N.V.P. (yes vs. no) | −0.876 | 0.290 | 9.139 | 0.003 | 2.4 | 1.361 | 4.235 |
Constant | −2.085 | 0.345 | 36.572 | 0.000 | 0.124 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Manolescu, L.S.C.; Zugravu, C.; Zaharia, C.N.; Dumitrescu, A.I.; Prasacu, I.; Radu, M.C.; Letiția, G.D.; Nita, I.; Cristache, C.M.; Gales, L.N. Barriers and Facilitators of Romanian HPV (Human Papillomavirus) Vaccination. Vaccines 2022, 10, 1722. https://doi.org/10.3390/vaccines10101722
Manolescu LSC, Zugravu C, Zaharia CN, Dumitrescu AI, Prasacu I, Radu MC, Letiția GD, Nita I, Cristache CM, Gales LN. Barriers and Facilitators of Romanian HPV (Human Papillomavirus) Vaccination. Vaccines. 2022; 10(10):1722. https://doi.org/10.3390/vaccines10101722
Chicago/Turabian StyleManolescu, Loredana Sabina Cornelia, Corina Zugravu, Corneliu Nicolae Zaharia, Anca Irina Dumitrescu, Irina Prasacu, Mihaela Corina Radu, Goraneanu Draghici Letiția, Irina Nita, Corina Marilena Cristache, and Laurentia Nicoleta Gales. 2022. "Barriers and Facilitators of Romanian HPV (Human Papillomavirus) Vaccination" Vaccines 10, no. 10: 1722. https://doi.org/10.3390/vaccines10101722
APA StyleManolescu, L. S. C., Zugravu, C., Zaharia, C. N., Dumitrescu, A. I., Prasacu, I., Radu, M. C., Letiția, G. D., Nita, I., Cristache, C. M., & Gales, L. N. (2022). Barriers and Facilitators of Romanian HPV (Human Papillomavirus) Vaccination. Vaccines, 10(10), 1722. https://doi.org/10.3390/vaccines10101722