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Original paper

Assessment of awareness of human papillomavirus infection impact on oral cavity among patients

Justyna Oleszkiewicz-Śpiołek
1
,
Paulina Adamska
1
,
Giulia Marvaso
2, 3
,
Barbara A. Jereczek-Fossa
2, 3
,
Piotr Wychowanski
4
,
Anna Starzyńska
1

1.
Department of Oral Surgery, Medical University of Gdansk, Gdansk, Poland
2.
Division of Radiotherapy, IEO European Institute of Oncology, IRCCS, Milan, Italy
3.
Department of Oncology and Hemato-oncology, University of Milan, Milan, Italy
4.
Department of Oral Surgery, Medical University of Warsaw, Warsaw, Poland
Adv Dermatol Allergol 2021; XXXVIII (6): 985–993
Online publish date: 2020/07/23
Article file
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Introduction

Human papillomavirus (HPV) is a virus from the papil-lomoviridae group of DNA viruses. There are as many as 150 types of this virus and we can divide them into two groups based on cancer risk: low-risk human papillomavirus (LR HPV) and high-risk human papillomavirus (HR HPV) [13]. HPV LR serotypes with a low oncogenic risk are most often associated with benign lesions on mucous and cutaneous membranes e.g. leukoplakia, erythroplakia, erythroleukoplakia, Lewandowsky-Lutz dysplasia (Epidermodysplasia verruciformis, EV), focal epithelial hyperplasia, condylomata acuminata or warts (cutaneous, mucous membranes). The following HPV LR types are responsible for these lesions: 1, 2, 3, 4, 6, 7, 10, 11, 13, 16, 18, 30, 31, 32, 33, 34, 35, 40, 42, 43, 44, 45, 52, 53, 54, 55, 57, 59, 61, 62, 64, 66, 68, 69, 71, 72, 73, 81, 83, 84, 89 and 120 [47]. Whereas HPV HR serotypes with a high oncogenic risk include HPV 2, 3, 6, 11, 13, 16, 18, 26, 31, 32, 33, 35, 39, 45, 51, 52, 53, 56, 57, 58, 59, 66 67, 68, 69, 70, 73 and 82. HPV high-risk types 16 and 18 are the most common aetiological factors of oral squamous cell carcinoma. Serotypes HPV 16 are responsible in 66–82% and HPV 18 in 26–34% for the presence of HPV-positive oral cancer [5, 8, 9].

The main aetiological factors of head and neck cancer, including oral cancer, are smoking and alcohol consumption. Tobacco-dependent oral cancer mainly affects people over 50 years of age. A worrying trend is increasing occurrence of behaviours in younger age groups. In this population, the presence of HPV infection with serotypes 16 and 18 is more frequent. They are also responsible for the occurrence of cervical cancer in females [10]. During chronic HPV infection, the risk of cervical cancer increases almost 500 times. The presence of HPV infection is necessary for the development of cancer, however not every patient with HPV develops cancer [11]. The frequency of HPV infection is higher in males than in females [12]. The infection may occur due to early sexual initiation, large number of sexual partners, poor hygiene or via shared underwear or towels. People at risk of HPV infection are females using oral hormonal contraception, and those who are immunocompromised and poorly nourished. Some sexual behaviours, including oral sex, are closely related to the HPV transmission from the oral cavity and the genitals. Oral HPV infection is less frequent than genital HPV [7, 13]. Immunodeficiency (e.g. due to HIV infection) or smoking are associated with an increased risk of oral infection. Persistent HPV infection plays a key role in the development of HPV-dependent diseases [14].

Differentiation of oral squamous cell carcinoma associated with HPV infection is clinically relevant because there is a different response to treatment. This is the subject of an ongoing debate as it has been shown that the treatment of oral cancer associated with HR serotypes and localized in the oral part of the throat or root of the tongue has a better clinical prognosis [15, 16]. There are many studies on the presence of HPV and its effect on the development of oral cancer. Conducting education and prevention of HPV infection is aimed at increasing awareness among patients, which may result in earlier detection of the disease [4, 1720].

Aim

The purpose of the study was to assess patients’ awareness of the impact of HPV infection on oral health.

Material and methods

This was a prospective study of dental patients who were treated in the Department of Oral Surgery at the Medical University of Gdańsk (Gdansk, Poland) from January to February 2019. Patients reported for mandibular third molar odontectomy.

Inclusion criteria were as follows: Polish-speaking patients over 18 years old. Exclusion criteria were as follows: people with limited Polish language knowledge and under 18 years old. Participation was voluntary. Full anonymity was maintained. Written consent was obtained from all participants. Completion of the questionnaire took about 15 min.

The questionnaire form consisted of four sociodemographic questions and thirteen HPV-specific questions. The questionnaire was an original idea and was prepared on the basis of available literature [15, 21]. This group of questions contained 5 single-answer questions and 8 multiple-answer questions (Appendix 1). In the multiple-answer questions, a minimum of three responses were correct. The questions focused on HPV-related terminology, the routes of transmission, mucosal symptoms, lesions in the oral cavity, and methods of treatment. Respondents were asked to answer questions about risk factors for infection, the existence of a vaccine, how to prevent infections, and other diseases that may arise from the presence of HPV. The obtained results were examined in terms of the relationship between the age, sex and education of the respondents and the awareness of the impact of HPV infection on oral health. The respondents were divided into three groups based on age: up to 25 years old (group 1), from 26 to 40 (group 2) and above 41 years of age (group 3).

The research project was approved by the Independent Bioethics Committee for Scientific Research at the Gdansk Medical University (NKBBN/441/2019). All participants were informed about the use of their data for research purposes.

Statistical analysis

The obtained results were analysed statistically using the Statistica v. 13.3 software (StatSoft Inc. Tulsa, USA). Normal distribution was verified using the W. Shapiro-Wilk test. Comparisons between study groups were compared using a non-parametric test for the age of independent groups at the level of significance p ≤ 0.05.

Results

Three hundred and sixty-three people (average age: 21 years, range: 18–65) were included in the study. 58.13% of participants were females (211) and 41.87% were males (152). The respondents were divided into three groups based on age. The first group included 290 respondents, the second 59 and the last only 14. Majority of the participants (35.0%) lived in the countryside, 33.30% lived in the cities with > 300,000 inhabitants, 27.0% in the towns up to 100,000 inhabitants and only 4.70% were from the towns from 100,000 to 300,000. Results were described in Table 1.

Table 1

Comparison of the patient survey results (*multiple-choice question)

QuestionsAge groupsAll respondentsP-value
≤ 2526–40> 40
n%n%n%n%
HPV means:
 Human papillomavirus17761.033864.411178.5722662.260.299
 Herpes simplex virus3211.03915.2517.144211.57
 Varicella zoster virus20.6946.7800.0061.65
 Mumps virus10.3411.6917.1430.83
 I do not know7826.90711.8617.148623.69
HPV infection routes*:
 Being in one room with an infected person72.4111.6900.0082.200.280
 Sexual contact with an infected person16155.512482.761178.5719653.99
 From the mother to the foetus during delivery7124.481423.73321.438824.24
 Via placenta3612.41610.1700.004211.57
 Skin contact with an infected person206.901322.33214.29359.64
 Breast-feeding237.93813.5500.003154
 Contact with infected blood10435.861932.20214.2912534.43
 Via food237.93711.8600.00308.26
 Via droplets7726.5535.08214.298222.59
 Via inhalation00.0000.0000.0000.00
 I do not know9633.102033.9017.1410729.48
HPV infection risk factors*:
 Smoking tobacco3211.0335.0800.00359.640.212
 Using of public toilets10.342237.29428.57277.43
 Drinking alcohol103.44610.1700.00164.41
 Drinking a lot of caffeine93.1058.4700.00143.86
 Large number of sexual partners10937.592745.76642.8614239.12
 Oral sex8629.661322.03428.5710328.37
 Anal sex5820.001322.03428.577520.66
 Lack of regular gynaecological and dental follow-up8428.971830.51321.4310528.93
 Eating unwashed vegetables and fruits3813.10813.5600.004612.67
 Numerous childbirths136.2235.0800.00164.41
 Frequent genital infections7024.14711.86214.297921.76
 I do not know12944.481728.81428.5715041.32
HPV infection symptoms*:
 Vesicular lesions on the lips4615.86711.86428.575715.700.082
 Warts in the oral cavity, on hands, feet, genitals6221.382237.29857.149225.34
 Enlarged cervical lymph nodes248.281423.7300.003810.47
 Rash51.7258.4700.00102.75
 I do not know9733.35196.55428.5712033.06
HPV infection can be asymptomatic:
 Yes14148.621728.81750.0016545.450.023
 No134.481932.2017.14330.10
 I do not know13646.902338.98642.8616545.45
HPV lesions in the oral cavity look like…*
 White spots on the tongue, cheeks, palate9733.451621.12642.8611932.780.263
 Red and white spots on the tongue, cheeks, palate248.271322.03214.293910.74
 Red, sore, burning papulae on the cheeks, tongue, palate4716.20915.2500.005615.43
 Cauliflower eruptions on the tongue, cheeks, palate4515.521932.22428.576818.73
 Small vesicles on the inside of the lower lip3512.071525.2317.145114.05
 I do not know15553.452033.90642.8618149.86
The features of lesions caused by the HPV virus on the mucous membrane are*:
 Soft3411.7221.35214.29369.920.014
 Painless268.971510.1400.004111.29
 Painful6422.073020.27214.299626.46
 More often skin colour193.851510.1400.00349.37
 Itchy5611.342114.19214.297921.76
 Not itchy142.83138.7817.14287.71
 Cauliflower shape428.50149.4600.005615.43
 Flat153.0474.7317.14236.34
 Round367.29128.1117.143910.74
 Angular102.0210.6817.14123.31
 I do not know17861.381812.161071.4320656.75
HPV infection may be responsible for the development of oral cancer:
 Yes12442.76915.25535.7113838.02< 0.001
 No258.622644.0717.145214.33
 I do not know14148.622440.68857.1417347.65
HPV infection may be responsible for the development of the following neoplasm*:
 Cervical cancer9031.032237.28964.2912133.330.485
 Penile cancer268.9758.47537.71369.92
 Breast cancer175.86711.8600.00246.61
 Prostate cancer217.24813.5600.00297.99
 Head and neck cancer (tonsils, larynx, paranasal sinuses, oral cavity)13646.902644.06321.4316545.45
 Papillomatosis of the airway5511.021322.0300.006818.73
 Lung cancer134.48610.1700.00195.23
 Progressive melanoma10.3458.4700.0061.65
 I do not know14048.281627.12428.5716044.08
HPV infection prevention*:
 Frequent hand washing4615.8611.69214.294913.500.852
 Using condoms11238.621932.20750.0013838.01
 Loyalty to one sexual partner9031.032237.29857.1412033.06
 Regular visits to the dentist8830.3400.00321.439125.07
 Personal and oral hygiene10335.522033.89750.0013035.81
 Washing fruits and vegetables before eating4916.901016.9500.005916.25
 Drinking boiled water144.83711.8600.00215.79
 Getting vaccinated3612.41915.2500.004512.40
 I do not know12643.451932.20214.2914740.50
Is there an HPV vaccine?
 Yes, but it is not obligatory9532.761322.03857.1411631.960.670
 Yes, and it is an obligatory vaccination (in Poland)165.52813.5617.14256.89
 No258.621627.1200.004111.29
 I do not know15453.102237.29535.7118149.86
Is there is an HPV test?
 Yes13546.551423.73535.7115442.420.002
 No144.831627.12321.43339.10
 I do not know14148.622949.15642.8617648.48
HPV infection treatment*:
 Antibiotics248.2811.6900.00257.71< 0.001
 Antiviral drugs3010.341118.64535.714612.67
 Surgery113.79813.56214.29215.78
 Infection is incurable, but the skin lesions can be removed7024.141627.1217.147721.21
 Laser therapy155.1723.3917.14184.96
 Burning off10.3435.0800.0041.10
 Cryotherapy41.3800.0000.0041.10
 I do not know13546.551830.51535.7115843.53

We demonstrated statistically relationships between the respondents’ sex and their knowledge of what HPV is (p = 0.011), the fact that HPV infection can be asymptomatic (p = 0.018), that HPV infection may be responsible for the development of oral cancer (p = 0.032;), there is an HPV vaccine (p < 0.001) and how to prevent infection (p < 0.001). Overall, our female respondents were more aware.

We found statistically differences between age groups. Younger patients were more aware that HPV infection may be responsible for the development of oral cancer (p = 0.007; in group 1), HPV infection methods (p < 0.001; in group 2) and information about the characteristics of the lesions caused by the HPV on the mucous membrane (p < 0.001; in group 2). Older respondents were more aware how to prevent infection (p = 0.044; in group 3).

We observed statistically relationships between the respondents’ education and their knowledge of the symptoms of HPV infection (p < 0.001), the fact that HPV infection can be asymptomatic (p = 0.010), information about what diseases can HPV infection contribute to (p = 0.044), the risk factors for HPV infection (p = 0.027), that there is a human papillomavirus test (p = 0.011) and vaccine (p = 0.048), how to prevent infection (p < 0.001) and the characteristics of the mucous membrane lesions caused by the HPV (p < 0.001). Overall, patients with higher education had more correct responses to our survey questions.

In terms of the participants’ residence (village or city/town), we obtained statistically relationships with their answers regarding the prevention of HPV infections (p = 0.023). City dwellers demonstrated more knowledge on this subject.

Most respondents (62.30%) knew what HPV was. Participants aged above 40 years old were more aware (group 1: 61.03%; group 2: 64.41%; group 3: 78.57%). Almost one-third of the respondents (29.48%) did not know the mechanism of transmission. The second group were more aware that the sexual contact with an infected person was the most common cause of infection (group 1: 55.51%; group 2: 82.76%; group 3: 78.57%). Other infection routes mentioned included: from the mother to the foetus during delivery (group 1: 24.48%; group 2: 23.73%; group 3: 21.43%) and skin contact with an infected person (group 1: 6.90%; group 2: 22.33%; group 3: 14.29%). 58.68% of the respondents were aware about the HPV infection risk factors. Risk factors, which were the most frequently mentioned included: large number of sexual partners (group 1: 37.59%; group 2: 45.76%; group 3: 42.86%), lack of regular gynaecological and dental follow-up (group 1: 28.97%; group 2: 30.51%; group 3: 21.43%), oral sex (group 1: 29.66%; group 2: 22.03%; group 3: 28.57%), frequent genital infections (group 1: 24.14%; group 2: 11.86%; group 3: 14.29%) and anal sex (group 1: 20.00%; group 2: 22.03%; group 3: 28.57%). 33.06% of the patients did not know the symptoms of HPV infection (group 1: 33.35%; group 2: 6.55%; group 3: 28.57%). More than half of the respondents (56.75%, p = 0.014) could not identify what the mucous membrane lesions caused by HPV looked like (group 1: 53.45%; group 2: 33.90%; group 3: 42.86%). Participants aged up to 25 years old were more aware. 45.65% (p = 0.023) of respondents did not know that HPV infection could occur in the latent form (group 1: 51.38%; group 2: 71.79%; group 3: 50.00%). Participants aged above 40 years old were more aware (50.00%).

Almost half (47.65%; p < 0.001) did not know that HPV infection could lead to oral cancer (group 1: 48.62%; group 2: 40.68%; group 3: 57.14%). Participants aged up to 25 years old were more aware (42.76%). The following were mentioned most frequently as other HPV-related cancers/lesions: head and neck cancers (group 1: 46.90%; group 2: 44.06%; group 3: 21.43%), cervical cancer (group 1: 31.03%; group 2: 37.28%; group 3: 64.29%), papillomatosis of the airway (group 1: 11.02%; group 2: 22.03%; group 3: 0.00%) and penile cancer (group 1: 8.97%; group 2: 8.47%; group 3: 37.71%).

As many as 40.50% of our participants did not know how to protect themselves against an HPV infection. The following were mentioned most frequently as HPV infection prevention measures: using condoms (group 1: 38.62%; group 2: 32.20%; group 3: 50.00%), personal and oral hygiene (group 1: 35.52%; group 2: 33.89%; group 3: 50.00%) and loyalty to one sexual partner (group 1: 31.03%; group 2: 37.29%; group 3: 57.14%). Participants above 40 years old were more aware (85.71%). 68.04% of the respondents gave wrong answer about the possibility of vaccination against HPV (group 1: 67.24%; group 2: 77.97%; group 3: 42.86%).

The existence of a diagnostic test detecting the presence of a virus in the body was reported only by 42% (p = 0.002) of respondents (group 1: 46.55%; group 2: 23.73%; group 3: 35.71%). 43.5% of the respondents had no idea about treatment methods (p < 0.001).

Discussion

Our survey conducted among the patients revealed their insufficient knowledge about the impact of HPV infection on oral health. Only one similar study was found in the PubMed database, and this issue was mentioned in 11 other studies. The work of Lewandowski et al. concerns knowledge about the viral infections and the impact of the risk of sexual behaviour on the occurrence of oral cancer [22]. That particular study involved 196 students who were 19–25 years of age and stated that HPV infection was primarily associated with squamous cell carcinoma of the cervix. Contrarily to our study, Lewandowski et al. had respondents just in one age group, up to 25 years. The role of HPV virus as a factor in the development of benign and malignant lesions was indicated by 59.7% of the respondents of Lewandowski et al., and by 61% of our respondents. The relationship between HPV infection and the occurrence of oral cancer was noted by 40.3% of the students interviewed by Lewandowski et al. and by 42.76% of our patients. In our study, oral sex, as a risk factor for HPV infection, was reported by 13.46% of our respondents, and by 34.7% of the respondents in the study by Lewandowski et al. The availability of the HPV vaccine as an element of the prevention of oral cancer is reported by 50.5% of the surveyed students, and among our patients this percentage is only 38.3% [22].

A study by Osazuwa-Peters et al. showed that 36% of respondents knew that HPV could contribute to oral cancer [23]. In addition, participants of the study indicated that HPV was mainly associated with cervical cancer. We obtained similar results. Pokharel et al. proved that 2 out of 3 respondents did not realize the relationship between oral sex and oral cancer [24]. Wroński et al. showed that patients were not aware of the relationship between oral cancer and oral sex or a large number of sexual partners [25]. In our study, the relationship between oral cancer and oral sex was identified by 13.46% of patients in the group up to 25 years of age, and 9.15% in the group of 26–40, and 14.81% over 40 years of age. In turn, the relationships between a large number of sexual partners were indicated by 17.06%, 19.15% and 22.22% of respondents respectively. In the work by Taberna et al., 40% of respondents indicated that HPV vaccination was important in the prevention of oral cancer [26].

There is a need to educate patients about the relationship between HPV infection and oral cancer, which was noticed by Dood et al. and Daley et al. [27, 28]. The respondents emphasized the role of medical personnel in expanding knowledge about HPV-positive oral cancer. According to interviewees, the information provided by medical personnel was more reliable than information from internet portals or the media.

The study by Bakr et al. conducted among students of dentistry and dental patients showed that their knowledge about the symptoms and risk factors (including HPV infection) of oral cancer was relatively low [29]. In the work of Formosa et al., 23% of respondents reported a connection between HPV infection and the occurrence of oral cancer [30]. In our study, it was 38% of the respondents. The results of a study conducted by Kram et al. among the parents of paediatric ward patients showed that 51.3% of respondents were aware of a vaccine against HPV and showed a desire to obtain additional information on vaccinations [31]. In our sample, 38.9% of patients knew about the availability of a vaccine against HPV. In addition, Kram et al. demonstrated that only 19.6% of respondents were aware of HPV infection as a risk factor for squamous cell carcinoma of the head and neck. Gichki et al. focused on issues related to HPV infection, and 53.1% of their respondents were aware that the HPV infection was influenced by sexual contact, however they did not know that HPV could be transmitted through mucous membranes and through the infected mother to the foetus [32]. In turn, as many as 59.4% of respondents did not realize that HPV infection had a significant impact on the development of potentially malignant disorders as well as malignant neoplasms of the head and neck. McBride et al. showed significant statistical differences between gender and knowledge about HPV infection and vaccines. Women had better general knowledge about HPV, and men about vaccination. In addition, the relationship between general knowledge and education, white race and higher earnings was demonstrated. Negative correlation was found in people over 65, among black and Asian races. Most participants (> 70%) knew that HPV might cause cervical cancer, but less people (14.9% to 31.5%) knew about the relationship between HPV and cancers of other parts of the body [33].

Conclusions

Our study suggests that patients’ awareness of the influence of HPV infections on oral health is limited. There is a need to educate patients about the risk factors for HPV infection and prevention methods, including the possibility of vaccinating themselves against HPV.

Conflict of interest

The authors declare no conflict of interest.

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McBride KR, Singh S , authors. Predictors of adults’ knowledge and awareness of HPV, HPV-associated cancers, and the HPV vaccine: implications for health education. Health educ Behav. 2018. 45:p. 68–76

Appendices

Appendix 1. The questionnaire form

Assessment of awereness of human papillomavirus infection on oral cavity among patients

Sociodemographic questions:

1) Gender:

  1. Male

  2. Female

2) Age….

3) Education:

  1. Primary education

  2. Secondary education

  3. Higher education

  4. Vocational education

4) Place of residence:

  1. Village

  2. A city of up to 100,000 inhabitants

  3. A city of up to 300,000 inhabitants

  4. A city with over 300,000 inhabitants

HPV-specific questions:

5) HPV means:

  1. Human papillomavirus

  2. Herpes simplex virus

  3. Varicella zoster virus

  4. Mumps virus

  5. I do not know

6) HPV infection routes*:

  1. Being in one room with infection person

  2. Sexual contact with infected person

  3. From the mother to the fetus during delivery

  4. Via placenta

  5. Skin contact with infected person

  6. Breast-feeding

  7. Contact with infected blood

  8. Via food

  9. Via droplets

  10. Via inhalation

  11. I do not know

7. HPV infection risk factors*:

  1. Smoking tobacco

  2. Using of public toilets

  3. Drinking alcohol

  4. Drinking a lot of caffeine

  5. Large number of sexual partners

  6. Oral sex

  7. Anal sex

  8. Lack of regular gynaecological and dental follow-up

  9. Eating unwashed vegetables and fruits

  10. Numerous childbirths

  11. Frequent genital infections

  12. I do not know

8. HPV infection symptoms*:

  1. Vesicular lesions on the lips

  2. Warts in the oral cavity, on hands, feet, genitals

  3. Enlarged cervical lymph nodes

  4. Rush

  5. I do not know

9. HPV infection can be asymptomatic:

  1. Yes

  2. No

  3. I do not know

10. HPV lesions in the oral cavity look like…*:

  1. White spots on the tongue, cheks, palate

  2. Red and white spots on the tongue, cheeks, palate

  3. Red, sore, burning papulae on the cheeks, palate

  4. Cauliflower eruptions on the tomgue, cheeks, palate

  5. Small vesicles on the inside of the lower lip

  6. I do not know

11. The features of lesions caused by the HPV virus on the mucous membrane are*:

  1. Soft

  2. Painless

  3. Painful

  4. More often skin colour

  5. Itchy

  6. Not itchy

  7. Cauliflower shapes

  8. Flat

  9. Round

  10. Angular

  11. I do not know

12. HPV infection may be responsible for the development of oral cancer:

  1. Yes

  2. No

  3. I do not know

13. HPV infection may be responsible for the development of the following neoplasm*:

  1. Cervical cancer

  2. Penile cancer

  3. Breast cancer

  4. Prostate cancer

  5. Head and neck cancer (tonsils, larynx, paranasal sinuses, oral cavity)

  6. Papilomatosis of the airway

  7. Lung cancer

  8. Progressive melanoma

  9. I do not know

14. HPV infection prevention*:

  1. Frequent hand washing

  2. Using condoms

  3. Loyalty to one sexual partner

  4. Regular visists to the dentist

  5. Personal and oral hygiene

  6. Washing fruits and vegetables before eating

  7. Drinking boiled water

  8. Getting vaccinated

  9. I do not know

15. Is there an HPV vaccine?

  1. Yes, but it is not obligatory

  2. Yes, and it is an obligatory vaccination (in Poland)

  3. No

  4. I do not know

16. Is there an HPV test?

  1. Yes

  2. No

  3. I do not know

17. HPV infection treatment*:

  1. Antibiotics

  2. Antiviral drugs

  3. Surgery

  4. Infection is incurable, but the skin lesions can be removed

  5. laser therapy

  6. Burning off

  7. Cryotherapy

  8. I do not know

*Multiple-answer question – a minimum of three responses are correct.

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