Knowledge about human papillomavirus transmission and prevention among physicians in Rio de Janeiro state, Brazil

SUMMARY

OBJECTIVE:

This study aimed to assess physicians’ knowledge about human papillomavirus infection and its prevention.

METHODS:

Descriptive web-based survey with 15 objective questions targeted to physicians affiliated with the Regional Council of Medicine from Rio de Janeiro state, Brazil. Participants were invited by e-mail and the Council social networks, between January and December 2019.

RESULTS:

The study sample had 623 participants, with a median age of 45 years, predominantly women (63%). The most frequent specialties were Obstetrics and Gynecology (21.1%), Pediatrics (11.2%), and Internists (10.5%). Concerning human papillomavirus knowledge, 27.9% of the participants were able to identify accurately all possible forms of transmission, and none of them could recognize all the risk factors of infection. Nevertheless, 95% recognized that asymptomatic infection could occur in both sexes. Regarding knowledge about clinical manifestations, diagnosis, and screening, only 46.5% were able to identify all human papillomavirus-related cancers, 42.6% were aware of the periodicity of Pap smears, and 39.4% indicated that serological test was not adequate for diagnosis. The recommended age group for human papillomavirus vaccination was recognized by 94% of the participants, as well as the need for a Pap smear and the use of condoms, even after vaccination.

CONCLUSIONS:

There is good knowledge about prevention and screening for human papillomavirus infections; many gaps were identified regarding transmission, risk factors, and associated diseases among physicians in Rio de Janeiro state.

KEYWORDS:
Papillomaviridae; Uterine cervical neoplasms; Genital neoplasms, female; Papillomavirus vaccines; Knowledge; Physicians

INTRODUCTION

Cervical cancer is a preventable disease, which is also curable if detected early and adequately treated. Nevertheless, it remains the fourth most common cancer among women globally and is expected to increase among young, undereducated women in the world’s poorest countries. The World Health Organization (WHO) launched the first global health strategy for the elimination of cervical cancer as a public health problem, and one of the goals is to reduce knowledge gaps concerning HPV infection¹. Additionally, HPV is involved in other cancers, such as anogenital and oropharyngeal ones, all of them susceptible to prevention by vaccine².

The success of HPV prevention programs will depend on whether health care professionals recommend the vaccine to patients. They influence the decision-making of patients and guardians, minimize vaccination barriers, and increase its acceptability³.

The knowledge on HPV and related cancers is developed throughout medical education and will be essential to physicians, especially those dealing with HPV malignant lesions at different levels of care—health counseling and education, prevention by vaccination and screening, diagnosis, treatment, and recovery⁴.

In Brazil, cervical cancer is still an important cause of cancer and death⁵. Urgent and bold action is needed to scale up and sustain evidence-based interventions. The identification of knowledge gaps among physicians can support proposals for improving medical education, reduce negative beliefs, and promote adherence to vaccination and other HPV prevention methods, contributing to HPV incidence reduction and cervical cancer control¹.

The objective of the study was to assess physicians’ knowledge about HPV infection and its prevention in Rio de Janeiro (RJ) state, Brazil.

METHODS

The study was approved by the Faculty of Medicine Ethics Committee from UFF (CAAE14660613.2.0000.5243) on May 20, 2013. All respondents were instructed about the goals of the study, and all of them filled out written online-administered informed consent. Participation was anonymous and voluntary, and the confidentiality of data was kept throughout the study. Participants were not involved in the development of this study.

We conducted a survey targeted to all physicians registered on “Conselho Regional de Medicina do RJ (CREMERJ)” between January and December 2019. Participants were invited by e-mail and social networks, such as Facebook.

Sample size calculations were based on a 70% estimated HPV knowledge⁶–⁸, according to previous studies⁶–⁸, with a 5% precision rate and a 95% confidence level. Considering a population of 60,000 physicians in RJ state⁹, we estimated a sample of 321 participants.

Participants completed a web-based survey (Google Forms) with 15 questions, including demographic data (gender, age), time since graduation, post-graduation (yes or not), university (public or private), and specialty (Internal Medicine, Pediatrics, Obstetrics/Gynecology, Urology, Dermatology, others). There were some closed questions (yes/not) requiring a single answer; others had multiple answers format, and a few had open fields.

Questions about HPV knowledge involved transmission (type of sexual intercourse, transplacental, and delivery routes), risk factors (partnership, toilet items, use of condoms and oral contraceptives, and age at sexarche), clinical presentation (warts and HPV-related cancers), cervical screening (frequency, technique, and interpretation), and HPV-vaccine recommendations (age and need of cervical screening).

Knowledge on HPV transmission, types of cancer, PAP smear, and serology was compared among specialties, and differences in proportions of total hits were tested using chi-square tests.

Data were entered and analyzed using SPSS Statistics version 23. Descriptive analysis used means or median for continuous variables and proportions for categorical ones. We described percentages of correct answers and percentages of total correct items when appropriate.

RESULTS

We obtained 623 answers, representing 1% of RJ physicians. Participants, whose median age was 45 years, were mostly women, with a postgraduate degree, and graduated for more than 10 years. Obstetricians/Gynecologists (OBGyn) comprised the most frequent specialty. A minority declared to be vaccinated against HPV was mostly women (Table 1).

Table 1
Sociodemographic profile, Rio de Janeiro state physicians (n=623), 2019.

Variables		n (%)
Age		45 (median)
Sex
	Female	392 (63)
	Male	230 (37)
Graduation
	Graduates	95 (15,3)
	Postgraduates	527 (84.7)
Time since graduation
	1–4 years	110 (17.7)
	5–10 years	80 (12.9)
	>10 years	432 (69.5)
Specialty
	Internal medicine	65 (10.5)
	Dermatology	33 (5.3)
	Gastroenterology	20 (3.2)
	Gynecology and obstetrics	131 (21.1)
	Pediatrics	70 (11.2)
	Urology	19 (3.1)
	Others	285 (45.8)
Public universities
	UFFa	96 (15.4)
	UFRJb	98 (15.7)
	UERJc	44 (7.1)
	UNIRIOd	54 (8.7)
Private universities
	FTESMe	67 (10.8)
Vaccinated against HPV
	Yes	138 (22.2)
Complete vaccination scheme
	Yes	121 (19.5)

• ^a
  Universidade Federal Fluminense
• ^b
  Universidade Federal do Rio de Janeiro
• ^c
  Universidade do Estado do Rio de Janeiro
• ^d
  Universidade Federal do Estado do Rio de Janeiro
• ^e
  Fundação Técnico-Educacional Souza Marques.

Regarding HPV knowledge, the item on clinical manifestations had the highest percentage of participants who answered all questions correctly. In contrast, none of the participants answered all risk factors correctly. As to transmission, this percentage was 30% (Table 2).

Table 2
Knowledge about human papillomavirus, among Rio de Janeiro state physicians (n=623), 2019.

Aspect of knowledge		Correct answers n (%)
Genital-genital		612 (98.4)
Oral-genital		541 (87.0)
Anal-genital		572 (92.0)
Transmission
	Manual-genital	315 (50.6)
	Transplacental	512 (82.3)
	Transvaginal delivery	438 (70.4)
	All answers are correct	185 (29.7)
	Toilet seat	567 (91.2)
	Share underwear and towels	462 (74.3)
	Sex without condoms	613 (98.6)
Risk situation
	Oral contraceptives	605 (97.3)
	Sex before 18 years old	0
	Share glasses and cutlery	604 (97.1)
	Multiple sex partners	577 (92.8)
	Partner with multiple partners	553 (88.9)
	Pool bath	619 (99.5)
	All answers are correct	0
	Pruritus	590 (94.9)
Clinical manifestations
	Bleeding	605 (97.3)
	Wart	600 (96.5)
	Pain	600 (96.5)
	Discharge	606 (97.4)
	All answers are correct	558 (89.7)
Asymptomatic occurrence		611 (98.2)
Asymptomatic transmission		594 (95.5)
Occurrence in both sexes		620 (99.7)
	Anal	490 (78.8)
	Oral	139 (60.4)
Types of cancer-associated
	Cervical	545 (87.6)
	Oropharynx	435 (69.9)
	Penile	514 (82.6)
	Vaginal	440 (70.7)
	Vulvar	469 (75.4)
	All answers are correct	289 (46.5)
Cervical cytology (PAP test)
	Test performed to detect changes in cervical cells	540 (86.8)
	Main strategy for detecting precursor lesions and cervical cancer	563 (90.5)
	Collection involves peeling the outer and inner surfaces of the cervix	498 (80.1)
	Performed by 25- and 64-year-old women who have or had a sexual life	482 (77.5)
	After two first annual exams with normal results, perform every 3 years	327 (52.6)
	All answers are correct	265 (42.6)
Diagnosis by serology		245 (39.4)
HPV vaccine
	Recommended age	587 (94.4)
	Need to realize PAP	618 (99.4)
	Need to use condoms	618 (99.4)

Less than half were right about HPV-related cancers. The majority are aware of uterine cervix cancer, and the lowest percentage was of oral cancer (Table 2).

Notably, 60% wrongly considered serological tests for diagnosis. The majority recognized the physiopathological basis of Pap smear. Despite this, only 42.6% correctly answered all the questions. In relation to the HPV vaccine, knowledge about age and recommendations was almost universal (Table 2).

OBGyn physicians performed better on PAP questions, but almost 30% did not answer all the items correctly (p<0.01). Urologists had the best score on HPV-related cancers, followed by OBGyn and dermatologists (p=0.04). OBGyn and urologists had better results than other specialties. There was no difference for transmission questions (p=0.13) (Table 3).

Table 3
Comparison of the number of correct answers about human papillomavirus outcomes, prevention, and diagnosis according to the specialties, Rio de Janeiro state physicians (n=623), 2019.

Specialty	Transmission	Types of cancer	PAP smear	Diagnosis by serology
	n (%)	n (%)	n (%)	n (%)
Gynecology and obstetrics	36 (27.5)	73 (55.7)	93 (71.0)	83 (63.4)
Internal medicine	18 (27.7)	24 (36.9)	33 (50.8)	14 (21.5)
Urology	12 (63.2)	13 (68.4)	1 (5.3)	12 (63.2)
Pediatrics	20 (28.6)	25 (36.6)	15 (21.4)	21 (30.0)
Gastroenterology	5 (27.3)	5 (36.4)	3 (18.2)	7 (36.4)
Dermatology	11 (33.3)	17 (51.5)	8 (24.2)	13 (39.4)
Others	83 (29.1)	129 (45.3)	110 (38.6)	96 (33.7)
p-value	0.13	0.04 *	<0.01 *	<0.01 *

• ^*
  Bold indicates statistically significant p-values.

DISCUSSION

In our study, physicians’ knowledge about HPV transmission was low, without differences among specialties. Although nearly 75% correctly marked the main routes of transmission, 25% wrongly identified non-related events. Knowledge about risk factors was good, except age at sexarche, but none of the participants could recognize all the risk factors. Most of them were able to identify the main clinical manifestations and the virus pathogenesis. There was a good perception of HPV infection and warts, but less than half of the participants correctly associated all HPV-related cancers, of which oral cancers being the less recognized ones. Finally, for the HPV vaccine, knowledge was almost universal.

Other studies confirmed the understanding of HPV as a sexually transmitted infection (STI) and gaps in knowledge about transmission, related diseases, and vaccination⁴,⁶–⁸,¹⁰–¹⁷.

It was noteworthy that none of the RJ physicians recognized early sexarche as a risk factor. In New Zealand, this question had a 73.8% score of correct answers⁶. The transplacental route was wrongly assigned by almost 20.0% of participants, a mistake also reported among Italian general practitioners (13.0%)¹².

The relationship between HPV and oral cancers, like our results, had one of the lowest scores in several studies¹⁰,¹²,¹³,¹⁵,¹⁶. Besides cervical cancer, knowledge about other HPV-related cancers was also low¹¹,¹². In contrast, physicians in RJ know more about warts than those in some other places⁶,¹¹,¹²,¹⁴.

More than half of the RJ doctors wrongly indicated serological tests for viral diagnosis. We also observed a lack of knowledge about the Brazilian cervical cancer screening protocol. Among ObGyn physicians, we found a better understanding of Pap test and HPV diagnosis, in agreement with Canadian studies¹⁸,¹⁹.

As to the HPV vaccine, 94.4% of RJ physicians were aware of the recommended age, while other studies showed lower scores: in Polonia, only 24.9%¹³; in Liguria, Italy, 73.7%⁷; in Italy, among general practitioners, 87.0%¹²; in Lebanon, 81.5%²⁰; and in the USA, 56.0% (family physicians) and 85.0% (pediatricians)²¹. Like our results, more than 90% of Irish physicians know that cervical cancer screening must continue in vaccinated women¹¹, but, in a study from Saudi Arabia, only 59.0% had this knowledge¹⁷.

Health care providers (HCPs) disseminate sexual health and prevention information to patients and their parents, especially concerning vaccination. Educational interventions are primarily directed at patients and parents rather than HCPs, despite evidence that provider recommendation is a key determinant of vaccine uptake¹⁰.

Along with cervical screening programs implemented by the Brazilian government, two vaccines, a bivalent and a quadrivalent one, are available in the National Immunization Program for females (9–14 years old) and males (11–14 years old) in a two-dose schedule²². However, a decrease in uptake has been observed: in 2014, 87% of Brazilian municipalities reached the target for the first dose but only 32% for the second dose²³.

The identification of knowledge gaps can support proposals for improving medical education content¹⁰. Students from health care courses in RJ state had difficulty to recognize all risk factors of HPV infection²⁴. We recommend additional education about HPV infection and prevention. Medical societies are recommended to offer continuous education for graduated professionals²¹.

Considering the study limitations, the sample represented only 1% of the RJ medical population, i.e., 59,366 professionals⁹. Mean age was similar, but females had a higher frequency (63%) than that of the State (50.8%). The sample size was adequate, but it was not random, allowing selection biases.

Our questionnaire used a closed question for specialties, offering five options, including “other”, which represented 45.8% of the answers. The four most common specialties in Brazil are Internal Medicine (11.2%), Pediatrics (10.3%), General Surgery (8.9%), and ObGyn (8%), while Dermatology represented 2.2% and Urology 1.4%⁹. Our sample distribution was adequate for Internal Medicine and Pediatrics, but ObGyn was overrepresented.

Although partially limited by selection and participation biases, this study confirmed gaps in HPV knowledge.

CONCLUSION

There is good knowledge about prevention and screening for HPV infections. Many gaps were identified regarding transmission, risk factors, and associated diseases among physicians in RJ state.

• Funding: none.

ACKNOWLEDGMENTS

We thank Conselho Regional de Medicina do Estado do Rio de Janeiro (CREMERJ) for publicizing our study online for the Rio de Janeiro physicians and associations.

REFERENCES

• ¹
  World Health Organization (WHO). Global strategy to accelerate the elimination of cervical cancer as a public health problem [Internet]. Geneva: World Health Organization; 2020. [cited on 2021 Nov 4] Available from: https://www.who.int/publications/i/item/9789240014107
  » https://www.who.int/publications/i/item/9789240014107
• ²
  Zhou JZ, Jou J, Cohen E. Vaccine strategies for human papillomavirus-associated head and neck cancers. Cancers (Basel). 2021;14(1):33. https://doi.org/10.3390/cancers14010033
  » https://doi.org/10.3390/cancers14010033
• ³
  Gilkey MB, Calo WA, Moss JL, Shah PD, Marciniak MW, Brewer NT. Provider communication and HPV vaccination: the impact of recommendation quality. Vaccine. 2016;34(9):1187-92. https://doi.org/10.1016/j.vaccine.2016.01.023
  » https://doi.org/10.1016/j.vaccine.2016.01.023
• ⁴
  Rosberger Z, Krawczyk A, Stephenson E, Lau S. HPV vaccine education: enhancing knowledge and attitudes of community counselors and educators. J Cancer Educ. 2014;29(3):473-7. https://doi.org/10.1007/s13187-013-0572-z
  » https://doi.org/10.1007/s13187-013-0572-z
• ⁵
  Ministério da Saúde. Instituto Nacional de Câncer José Alencar Gomes da Silva. Estimativa/2020 – Incidência de Câncer no Brasil [Internet]. Rio de Janeiro: INCA, 2019. p. 120. [cited 2021 Nov 4]. Available from: https://www.inca.gov.br/sites/ufu.sti.inca.local/files/media/document/estimativa-2020-incidencia-de-cancer-no-brasil.pdf
  » https://www.inca.gov.br/sites/ufu.sti.inca.local/files/media/document/estimativa-2020-incidencia-de-cancer-no-brasil.pdf
• ⁶
  Sherman SM, Bartholomew K, Denison HJ, Patel H, Moss EL, Douwes J, et al. Knowledge, attitudes and awareness of the human papillomavirus among health professionals in New Zealand. PLoS One. 2018;13(12):e0197648. https://doi.org/10.1371/journal.pone.0197648
  » https://doi.org/10.1371/journal.pone.0197648
• ⁷
  Trucchi C, Restivo V, Amicizia D, Fortunato F, Manca A, Martinelli D, et al. Italian health care workers’ knowledge, attitudes, and practices regarding human papillomavirus infection and prevention. Int J Environ Res Public Health. 2020;17(15):5278. https://doi.org/10.3390/ijerph17155278
  » https://doi.org/10.3390/ijerph17155278
• ⁸
  Xenaki D, Plotas P, Michail G, Poulas K, Jelastopulu E. Knowledge, behaviours and attitudes for human papillomavirus (HPV) prevention among educators and health professionals in Greece. Eur Rev Med Pharmacol Sci. 2020;24(14):7745-52. https://doi.org/10.26355/eurrev_202007_22277
  » https://doi.org/10.26355/eurrev_202007_22277
• ⁹
  Scheffer M, Cassenote A, Guilloux AGA, Miotto BA, Mainard GM, Matijasevich A, et al. Medical demography in Brazil 2018 [Internet]. São Paulo: FMUSP, CFM, Cremesp. 2018. p. 286. [cited 2021 Nov 2]. Available from: https://jornal.usp.br/wp-content/uploads/DemografiaMedica2018.pdf
  » https://jornal.usp.br/wp-content/uploads/DemografiaMedica2018.pdf
• ¹⁰
  Leung SOA, Akinwunmi B, Elias KM, Feldman S. Educating healthcare providers to increase human papillomavirus (HPV) vaccination rates: a qualitative systematic review. Vaccine X. 2019;3:100037. https://doi.org/10.1016/j.jvacx.2019.100037
  » https://doi.org/10.1016/j.jvacx.2019.100037
• ¹¹
  McSherry LA, O’Leary E, Dombrowski SU, Francis JJ, Martin CM, O’Leary JJ, et al. Which primary care practitioners have poor human papillomavirus (HPV) knowledge? A step towards informing the development of professional education initiatives. PLoS One. 2018;13(12):e0208482. https://doi.org/10.1371/journal.pone.0208482
  » https://doi.org/10.1371/journal.pone.0208482
• ¹²
  Signorelli C, Odone A, Pezzetti F, Spagnoli F, Visciarelli S, Ferrari A, et al. Infezione da papillomavirus umano e vaccinazione: conoscenze e ruolo dei medici di medicina generale. Epidemiol Prev. 2014;38(6 Suppl 2):88-92.
• ¹³
  Smolarczyk K, Pieta W, Majewski S. Assessment of the state of knowledge about HPV infection and HPV vaccination among Polish resident doctors. Int J Environ Res Public Health. 2021;18(2):551. https://doi.org/10.3390/ijerph18020551
  » https://doi.org/10.3390/ijerph18020551
• ¹⁴
  Pereira JEG, Gomes JM, Costa AS, Figueiredo FW dos S, Adami F, Santos EFS, et al. Knowledge and acceptability of the human papillomavirus vaccine among health professionals in Acre state, western Amazon. Clinics (Sao Paulo). 2019;74: e1166. https://doi.org/10.6061/clinics/2019/e1166
  » https://doi.org/10.6061/clinics/2019/e1166
• ¹⁵
  Lechner M, Vassie C, Kavasogullari C, Jones O, Howard J, Masterson L, et al. A cross-sectional survey of awareness of human papillomavirus-associated oropharyngeal cancers among general practitioners in the UK. BMJ Open. 2018;8(7): e023339. https://doi.org/10.1136/bmjopen-2018-023339
  » https://doi.org/10.1136/bmjopen-2018-023339
• ¹⁶
  Jackowska J, Bartochowska A, Karlik M, Wichtowski M, Tokarski M, Wierzbicka M. The knowledge of the role of papillomavirus—related head and neck pathologies among general practitioners, otolaryngologists and trainees. A survey-based study. PLoS One. 2015;10(10):e0141003. https://doi.org/10.1371/journal.pone.0141003
  » https://doi.org/10.1371/journal.pone.0141003
• ¹⁷
  Almazrou S, Saddik B, Jradi H. Knowledge, attitudes, and practices of Saudi physicians regarding cervical cancer and the human papilloma virus vaccine. J Infect Public Health. 2020;13(4):584-90. https://doi.org/10.1016/j.jiph.2019.09.002
  » https://doi.org/10.1016/j.jiph.2019.09.002
• ¹⁸
  Anderson S, Isaac A, Jeffery CC, Robinson JL, Isaac DM, Korownyk C, et al. Practices regarding human Papillomavirus counseling and vaccination in head and neck cancer: a Canadian physician questionnaire. J Otolaryngol Head Neck Surg. 2017;46(1):61. https://doi.org/10.1186/s40463-017-0237-8
  » https://doi.org/10.1186/s40463-017-0237-8
• ¹⁹
  Steben M, Durand N, Guichon JR, Greenwald ZR, McFaul S, Blake J. A national survey of Canadian adults on HPV: knowledge, attitudes, and barriers to the HPV vaccine. J Obstet Gynaecol Can. 2019;41(8):1125-33.e6. https://doi.org/10.1016/j.jogc.2019.05.005
  » https://doi.org/10.1016/j.jogc.2019.05.005
• ²⁰
  Abi Jaoude J, Khair D, Dagher H, Saad H, Cherfan P, Kaafarani MA, et al. Factors associated with human papilloma virus (HPV) vaccine recommendation by physicians in Lebanon, a cross-sectional study. Vaccine. 2018;36(49):7562-7. https://doi.org/10.1016/j.vaccine.2018.10.065
  » https://doi.org/10.1016/j.vaccine.2018.10.065
• ²¹
  Hswen Y, Gilkey MB, Rimer BK, Brewer NT. Improving physician recommendations for human papillomavirus vaccination: the role of professional organizations. Sex Transm Dis. 2017;44(1):42-7. https://doi.org/10.1097/OLQ.0000000000000543
  » https://doi.org/10.1097/OLQ.0000000000000543
• ²²
  Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Coordenação-Geral do programa Nacional de Imunizações. Informe técnico da ampliação da oferta das vacinas papilomavírus humano 6, 11, 16 e 18 – vacina HPV quadrivalente e meningocócica C (conjugada) [Internet]. Brasília: Ministério da Saúde; 2018. p. 39. [cited 2021 Nov 4]. Available from: https://portalarquivos2.saude.gov.br/images/pdf/2018/marco/14/Informe-T--cnico-HPV-MENINGITE.pdf
  » https://portalarquivos2.saude.gov.br/images/pdf/2018/marco/14/Informe-T--cnico-HPV-MENINGITE.pdf
• ²³
  Moura LL, Codeço CT, Luz PM. Cobertura da vacina papilomavírus humano (HPV) no Brasil: heterogeneidade espacial e entre coortes etárias. Rev Bras Epidemiol. 2021;24:e210001. https://doi.org/10.1590/1980-549720210001
  » https://doi.org/10.1590/1980-549720210001
• ²⁴
  Baptista AD, Simão CX, Santos VCGD, Melgaço JG, Cavalcanti SMB, Fonseca SC, et al. Knowledge of human papillomavirus and Pap test among Brazilian university students. Rev Assoc Med Bras. 2019;65(5):625-32. https://doi.org/10.1590/1806-9282.65.5.625
  » https://doi.org/10.1590/1806-9282.65.5.625

Publication Dates

• Publication in this collection
  21 Apr 2023
• Date of issue
  2023

History

• Received
  04 Oct 2022
• Accepted
  14 Nov 2022