Human Papillomavirus Infection in Pregnant Adolescentes: Is There an Association Between Genital and Mouth Infection?
Cavalcanti1, Silva2, Ferreira1, Neves2, Vanderborght3, Luiz4 and Torres1*
1Department of Oral Pathology and Diagnosis and Department of Clinic Odontologic, Dental School, Universidade Federal do Rio de Janeiro, Brazil
2Department of Gynecology and Obstetrics, Maternity School, School of Medicine, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil
3D' Or Institute for Research and Education, Rio de Janeiro, Brazil
4IESC, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
*Corresponding author: Prof. Sandra R Torres, PhD, Department of Oral Pathology and Diagnosis, Dental School, Universidade Federal do Rio de Janeiro (FO/UFRJ), Av. Carlos Chagas Filho 373 - Prédio do CCS - Bloco K - 2° andar - Sala 56. Ilha da Cidade Universitária - Rio de Janeiro/RJ - CEP: 21.941-902, Brazil, Tel: +55213938-2012, E-mail: email@example.com
Int J Oral Dent Health, IJODH-2-037, (Volume 2, Issue 4), Research Article; ISSN: 2469-5734
Received: October 30, 2016 | Accepted: December 10, 2016 | Published: December 12, 2016
Citation: Cavalcanti, Silva, Ferreira, Neves, Vanderborght, et al. (2016) Human Papillomavirus Infection in Pregnant Adolescentes: Is There an Association Between Genital and Mouth Infection?. Int J Oral Dent Health 2:037. 10.23937/2469-5734/1510037
Copyright: © 2016 Cavalcanti, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Introduction: The aim of this cross-sectional study was to verify the association of HPV infection in the cervix and the mouth of pregnant adolescents.
Methods: Clinical exam and smears of the cervix and the mouth were performed in thirty pregnant adolescents. Dental biofilm was collected for molecular evaluation. The cytology was analyzed using Bethesda criteria and the molecular evaluation by microarray assay. Associations of HPV infection with socio-demographic-behavioral characteristics and periodontal status were verified.
Results: The mean age of participants was 15.2 [± 1.3] years, and the mean pregnancy length was 28.8 [± 7.3] weeks. In the genital region, six (20%) subjects exhibited HPV-induced lesions. Cytological analysis showed HPV-induced cytophatic cells in 3 (10%) adolescents. Seventeen (56.7%) adolescents presented HPV DNA on the microarray assay. No HPV infection was detected in the mouth, either by clinical, cytological or molecular evaluation. All pregnant adolescents presented some degree of periodontal disease (n = 22 [73.3%] gingivitis and n = 8 [26.6%] periodontitis). Genital HPV infection was significantly more frequent in subjects with gingivitis (P < 0.05, Fisher exact test). There was no concordance between clinical exam and cytological/molecular assessment to identify the HPV infection in the genital area (clinical and cytological: P = 0.103; clinical and molecular: P = 0.198; cytological and molecular: P = 0.157; Kappa test).
Conclusion: The microarray assay was more sensitive to detect HPV infection in the cervix, when compared to clinical exam and cytological analysis. There was no association of the HPV infection in the genitalia and the mouth, in the studied population of pregnant adolescents.
Papilloma virus DNA probes, Adolescent, Pregnant women, Mouth, Periodontal diseases
Human Papillomavirus infection (HPV) is the most common sexually transmitted disease. The mouth has been reported as a frequent site for the infection, after the genital area . The association of the HPV infection in the genital and the mouth regions has been studied by many authors, with controversial results [2-15]. This association may be better observed in individuals who are more susceptible for HPV infection, like young individuals , homossexual males , and human immunodeficiency virus infected individuals . There are many reasons for infection susceptibility, such as hormonal changes [1,18], tissue immaturity [1,18], multiple sex partners, and some systemic diseases . Oral transmission may occur through orogenital sexual contact , oral-oral contact  and mother-fetus transmission .
The prevalence of HPV infection in the genital region varies from 5.9% to 81.7%, for adolescents [22,23]. During pregnancy, there is more vulnerability for HPV infection in the genital area of young women, than in older women . The prevalence of genital HPV infection in young pregnant women varies from 49% to 60%, in different countries [24-26].
Nearly 23% of the Brazilian healthy individuals are infected by the HPV in the oral mucosa . The HPV may infect the oral epithelium in a latent and asymptomatic form, or it may produce oral lesions. The virus has been detected in the site of periodontal disease of immune competent and immune suppressed individuals [28-31]. Thus, it has been suggested that the periodontum may be a reservoir for HPV in the mouth .
The controversial results about the association of the HPV infection in the mouth and the genital regions may be due to geographical reasons. Only few authors studied this association in a Brazilian population [2,6,12,24,25]. This study aimed to detect HPV infection in the cervix and the mouth of pregnant adolescents. An additional aim was to evaluate the concordance of clinical exam and cytological/molecular HPV methods to identify HPV infection.
This was a cross-sectional study in which pregnant adolescents attending the Maternity School of the Universidade Federal do Rio de Janeiro (UFRJ/Brazil) were evaluated for HPV infection in mouth and genital areas.
A convenience sample of adolescents seeking assistance for prenatal care, during the period of six months, represented the population of the study. All pregnant teenagers from the Maternity School of UFRJ were invited to participate in the study. Individuals were included if adolescent, aged between 10 and 19 years according World Health Organization, and agreed to participate in the study. Subjects were excluded if they presented any other genital infection. The research was approved by the institution review board at the University, and all subjects signed a consent form.
The pregnant adolescents were invited to participate in the study during the routine gynecological appointment. A complete examination of the genitalia and oral regions were performed by experienced gynecologist and dentist, respectively, to investigate for HPV infection. Clinical, socio-demographic and behavioral characteristics were collected from medical records and interview.
In the genital region, the external genital (minor and major labia), perianal and anal region were inspected. The internal genitalia was examined after the insertion of the speculum and the application of acetic acid 2%, in order to identify possible staining suggestive of HPV infection.
The oral exam was performed in a hospital gurney with a forehead light-emitting diode (LED) lamp. Acetic acid was not applied because it is not considered a good indicator of HPV infection in the oral tissues . A complete periodontal exam was performed by a trained periodontist, and the reliability of the evaluation was tested (P = 0.885, intra-class correlation coefficient [95% CI: 0.883-0.887]). The gingival index system , probing depth, clinical attachment level, and bleeding on probing were obtained and measured with a conventional North Carolina periodontal probe (Hu-Friedy, Chicago, IL, USA). Six sites per tooth were measured in a full mouth exam. Periodontal disease (gingivitis and periodontitis) was diagnosed through the evaluation of these parameters. Gingivitis was diagnosed when the supragingival bleeding was present in > 10% of the sites . Periodontitis was considered if the clinical attachment level was ≥ 5 mm , in at least 4 sites, and bleeding on probing was observed in 3 different teeth.
Cytology foam brushes were used to collect two samples from the uterine cervix and two from the mouth. Each sample collection was taken with six full turns of the brush. The first sample from the uterine cervix was spread on a slide and fixed in 70% alcohol for cytological analysis. The second sample was collected from the same region and placed in a tube containing 3 ml of the specimen transport medium (STM) buffer solution (Papillocheck® collection kit, Greiner Bio-One GmbH, Germany). The tube was cooled at 4 °C, until HPV genotyping.
In the mouth, the samples were taken from the dorsum of tongue and the area between hard and soft palate, with the same technique. The first sample was spread on a slide and fixed in alcohol, and the second sample taken from same area was placed in STM and cooled until genotyping.
Additionally, four subgingival biofilm samples were collected from the deepest sulcus sites (identified in the periodontal exam) from each subject. Prior to collection, supragingival plaque and saliva were removed from the teeth using sterile cotton rolls. A sterile 11-12 Gracey periodontal curette (Hu-Friedy, Chicago, IL, USA) was gently inserted into the periodontal pocket and the subgingival material was collected. The samples were stored in dry sterile tubes and kept at -80 °C, until analysis.
The slides of the cervical and oral samples were stained by the Papanicolau (Pap) method and were evaluated by a cytopathologist using the Bethesda criteria.
The samples in the frozen tubes were restored to room temperature. The cells were submitted to DNA purification using QIAamp DNA Mini Kit® protocol (Qiagen, Germany), according to the manufacturer's guidelines. The HPV genotyping was performed using the microarray assay test (PapilloCheck® microarray kit, Greiner Bio-One GmbH, Germany), which identifies 18 high risk and 6 low risk types of HPV (HPV 6, 11, 16, 18, 31, 33, 35, 39, 40, 42, 43, 45, 51, 52, 53, 56, 58, 59, 66, 68, 70, 73, 82, 44/55).
Descriptive data analysis was reported as the absolute frequency and percentage for categorical variables, and mean and standard deviation for the continuous variables. Fisher exact test was used to verify the differences between HPV presence in uterine cervix and in periodontal disease. Kappa test was used to correlate the results of the three methods of diagnosis for HPV infection (clinical, cytological and molecular). The p values ≤ 0.05 were considered statistically significant.
Thirty-one pregnant adolescents were recruited for the study, but one refused to participate. The mean (and standard deviation [SD]) age of the 30 included subjects was 15.2 [SD ± 1.3] years and the mean gestational period was 28.8 [SD ± 7.3] weeks. Social and behavioral characteristics are showed in table 1. The number of sexual partners reported by the subjects varied from 1 to 10 partners, with a mean of 2.4 partners [SD ± 2.3]. The practice of oral sex was reported by 18 (60%) of them, and the other 12 (40%) reported did not have this type of sex practice.
Table 1: Socio-demographic characteristics of the 30 pregnant adolescents. View Table 1
Clinical, cytological and molecular exams
In the clinical exam of the genital area, eight (23%) subjects presented HPV-induced lesions (condiloma accuminatum). Five of them showed lesions in the external genitalia and three in both external and internal genitalia.
In the cytological analysis of the uterine cervix, all the smears presented appropriated material for the evaluation. Three (10%) subjects presented HPV-induced cell changes in the cytological analysis of the uterine cervix. Two (6%) samples presented low grade squamous intraepithelial lesions and one (3%) slide showed atypical squamous cells of undetermined significance (ASC-US).
In the microarray assay of the uterine cervix, seventeen (56.7%) subjects were positive for HPV. One adolescent did not present conclusive cytology alterations for HPV infection (ASC-US), but was positive for HPV6 and HPV56 in the microarray assay (Papillocheck®). Fourteen (51.9%) of the 27 subjects that did not show HPV induced cell changes in the Pap test presented positive for HPV DNA (Table 2). The more prevalent subtype was HPV 16 (n = 4/23.5%), followed by the HPV 68 (n = 3/17.6%). Table 2 shows the different subtypes identified by the microarray test. Multiple infections were presented in eight (47.1%) subjects, and one of them exhibited five different HPV subtypes (high risk HPV 16, 31, 58, 39, 73).
Table 2: HPV infection evaluation in the 30 pregnant adolescents. View Table 2
In the mouth, no HPV-induced lesions were found in the clinical exam. In the cytological analysis, all the samples showed appropriate material for the evaluation, but none of them presented HPV-induced cytophatic cells. The microarray assay did not identify the DNA HPV in any oral smear sample.
Status of periodontal disease
None of the adolescents presented normal periodontal status. Table 3 shows the frequency of gingivitis and periodontitis in the studied population and the association with the microarray results from the uterine cervix. The genital HPV infection was significantly more frequent in subjects that showed gingivitis than those who did not present gingivitis (P = 0.04, Fisher exact test). This association was not found in those subjects who presented periodontitis.
Table 3: Periodontal status of 30 pregnant adolescents according to HPV infection in the cervix through the microarray results. View Table 3
One hundred and twenty subgingival biofilm samples were collected (the four deepest pocket per subject). The HPV was identified in one (0.08%) of the subgingival samples (low risk, HPV 6). Gingivitis was observed in the adolescent with a positive HPV in the gingival sulcus, but the site where HPV was detected presented normal clinical aspect. This adolescent who exhibited HPV in the biofilm also exhibited HPV in the uterine cervix (high risk, HPV 56).
Genital and mouth HPV infection association
There was no association of HPV infection in the uterine cervix with the infection in the mouth. The simultaneous presence of HPV infection in the genitalia and the tongue/palate area was not observed in any subjects.
There was no concordance between the clinical exam, the cytological exam and the molecular HPV assay to identify the HPV infection in the genital area (clinical and cytologic, P = 0.10; clinical and molecular, P = 0.19; cytologic and molecular, P = 0.15, Kappa test). The concordance between methods for HPV detection could not be tested in the oral mucosa, because none of them could detect the HPV infection. In the periodontum, the positive sample was not enough for correlation.
More than half of the pregnant adolescents in the present study presented HPV infection of the uterine cervix, but none of them presented HPV infection of the tongue/palate. There was no association between genital and oral HPV infection in the studied population. This is in agreement with other studies which evaluated older populations of pregnant women [10-11]. This association was reported only in one case of pregnant adolescent in the literature , but had never been studied in a group of pregnant adolescents.
The lack of association between the HPV infection in the mouth and the genital area has also been observed in other populations [10,12,13,15]. However, there are some studies that reported an association of HPV infection in these two regions [2,4-6,8,9,32]. Studies performed in the Brazilian population were performed in groups of non-pregnant women, men and heterosexual couples, and they are also controversial [2,6,12,24,25].
Some risk factors have been suggested for the concomitant infection in the genital area and the mouth, like orogenital sex practice [4,5,9,32], young age at first intercourse , and alcohol consumption . In this study, more than half of the adolescents reported oral sex practices, but HPV DNA was not found in any sample of their tongue/palate. Among the Brazilian studies that showed the association of HPV infection in the genitalia and the mouth, smoke was considered a risk factor in one study , but orogenital sex was not regarded as a risk factor .
Pregnancy has been pointed as a risk condition for HPV infection in the cervical region [8,22,24]. The present study was not designed for risk calculation; therefore, we did not have a control group of non-pregnant adolescents for comparison. However, almost half of the adolescents presented multiple high risk HPV DNA infections, which is higher than the frequency observed in other studies [37,38]. The HPV16 was the most prevalent subtype observed in the present study and in other studies .
The majority of the pregnant adolescents of the studied population did not show HPV-induced cytological changes in the uterine cervix, but over fifty percent of them had positive HPV DNA on the microarray assay. This is a common finding in other studies as well [22,39,40]. According to the Bethesda criteria, the cellular changes on smears of the cervix are not conclusive for the HPV absence. Molecular tests are best addressed to detect viral DNA.
There was no HPV infection in the mouth (tongue/palate) of pregnant adolescents in the clinical, cytological and molecular evaluation. Cytology is not considered the first choice method for the analysis of HPV infection in the mouth, when patients do not present lesions, and it does not seem to be a reliable screening technique in the clinically healthy oral mucosa . Furthermore, the oral sample collection may not be representative of the whole oral mucosa. Despite these arguments, the results of the three methods agreed upon the absence of the HPV infection in the mouth, in the studied population.
There are specific receptors in the gingival cells for estrogens . Hormonal peaks that occur in adolescence and pregnancy may change the immune response and thus influence the susceptibility and the resistance to infections in the periodontal tissues in these periods of the women’s life . Many studies showed controversial results in relation to the presence of HPV in the site of the periodontal disease [28,31,42,43]. In none of these studies, the oral sex habits was investigated and related to the HPV presence in the periodontum. In the only pregnant adolescent of this study that presented the HPV DNA in the biofilm, it was observed that she reported having oral sex one week before the sample collection.
The patient with positive HPV in the biofilm presented gingivitis, but not in the site of sample collection. Maybe the lack of association was a result of the non-advanced periodontal disease due, to young age. However, it was observed that subjects with HPV infection of the uterine cervix presented more gingivitis than those negative for HPV. Pregnant women are more susceptible for both gingivitis and for HPV infection in uterine cervix, because of the hormonal changes [23,42]. Thus, these findings are probably consequences of pregnancy, and may not be related among themselves.
This study had some limitations. Although it showed agreement with the studies that evaluated pregnant women, our sample size was relatively small and composed only by pregnant adolescents. Moreover, the young age of subjects limited the evaluation of some social and behavior characteristics that may be related to HPV infection, but needed more life time cumulative experience.
There was no association between the HPV infection in the genital and the mouth regions, in the studied population of pregnant adolescents. The methods used to detect HPV infection induced lesions showed concordance in the mouth, but not in the genital region.
Thanks to D' Or Institute for Research and Education, Rio de Janeiro, Brazil that funded this research.
Conflict of Interest
The authors disclose have no conflict of interest.
This study followed the principles of Helsinki declaration and was approved by Institutional ethics committee.
Schlecht NF, Burk RD, Nucci-Sack A, Shankar V, Peake K, et al. (2012) Cervical, anal and oral HPV in an adolescent inner-city health clinic providing free vaccinations. PLoS One 7: e37419.
Giraldo P, Goncalves AK, Pereira SA, Barros-Mazon S, Gondo ML, et al. (2006) Human papillomavirus in the oral mucosa of women with genital human papillomavirus lesions. Eur J Obs Gynecol Reprod Biol 126: 104-106.
Sanchez-Vargas LO, Díaz-Hernandez C, Martinez-Martinez A (2010) Detection of Human Papilloma Virus (HPV) in oral mucosa of women with cervical lesions and their relation to oral sex practices. Infect Agent Cancer 5: 25.
Peixoto AP, Campos GS, Queiroz LB, Sardi SI (2011) Asymptomatic oral human papillomavirus (HPV) infection in women with a histopathologic diagnosis of genital HPV. J Oral Sci 53: 451-459.
Termine N, Giovannelli L, Matranga D, Caleca MP, Bellavia C, et al. (2011) Oral human papillomavirus infection in women with cervical HPV infection: new data from an Italian cohort and a metanalysis of the literature. Oral Oncol 47: 244-250.
Zonta MA, Monteiro J, Santos Jr G, Pignatari AC (2012) Oral infection by the Human Papilloma Virus in women with cervical lesions at a prison in São Paulo, Brazil. Braz J Otorhinolaryngol 78: 66-72.
Du J, Nordfors C, Ahrlund-richter A, Sobkowiak M, Romanitan M, et al. (2012) Prevalence of Oral Human Papillomavirus Infection among Youth, Sweden. Emerg Infect Dis 18: 10-13.
Beder Ribeiro C, Ferrer I, Santos de Farias A, Fonseca DD, Morais Silva IH, et al. (2014) Oral and genital HPV genotypic concordance between sexual partners. Clin Oral Invest 18: 261-268.
Adamopoulou M, Vairaktaris E, Nkenke E, Avgoustidis D, Karakitsos P, et al. (2013) Prevalence of human papillomavirus in saliva and cervix of sexually active women. Gynecol Oncol 129: 395-400.
Smith EM, Ritchie JM, Yankowitz J, Wang D, Turek LP, et al. (2004) HPV prevalence and concordance in the cervix and oral cavity of pregnant women. Infect Dis Obstet Gynecol 12: 45-56.
Rintala M, Grenman S, Puranen M, Syrjanen S (2006) Natural history of oral papillomavirus infections in spouses: a prospective Finnish HPV Family Study. J Clin Virol 35: 89-94.
Xavier SD, Bussoloti Filho I, de Carvalho JM, Castro TM, Framil VM, et al. (2009) Prevalence of human papillomavirus (HPV) DNA in oral mucosa of men with anogenital HPV infection. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 108: 732-737.
Castro TM, Bussoloti Filho I, Nascimento VX, Xavier SD (2009) HPV detection in the oral and genital mucosa of women with positive histopathological exam for genital HPV, by means of the PCR. Braz J Otorhinolaryngol 75: 167-171.
Termine N, Giovannelli L, Matranga D, Perino A, Panzarella V, et al. (2009) Low rate of oral human papillomavirus (HPV) infection in women screened for cervical HPV infection in Southern Italy: A cross-sectional study of 140 immunocompetent subjects. J Med Virol 81: 1438-143.
Paaso AE, Louvanto K, Syrjänen KJ, Waterboer T, Grénman SE, et al. (2011) Lack of type-specific concordance between human papillomavirus (HPV) serology and HPV DNA detection in the uterine cervix and oral mucosa. J Gen Virol 92: 2034-2046.
Read TR, Hocking JS, Vodstrcil LA, Tabrizi SN, McCullough MJ, et al. (2012) Oral human papillomavirus in men having sex with men: risk-factors and sampling. PLoS One 7: e49324.
Kreimer AR, Alberg AJ, Daniel R, Gravitt PE, Viscidi R, et al. (2004) Oral human papillomavirus infection in adults is associated with sexual behavior and HIV serostatus. J Infect Dis 189: 686-698.
Smith EM, Swarnavel S, Ritchie JM, Wang D, Haugen TH, et al. (2007) Prevalence of human papillomavirus in the oral cavity/oropharynx in a large population of children and adolescents. Pediatr Infect Dis J 26: 836-840.
D'Souza G, Agrawal Y, Halpern J, Bodison S, Gillison ML (2009) Oral sexual behaviors associated with prevalent oral human papillomavirus infection. J Infect Dis 199: 1263-1269.
Kero K, Rautava J, Syrjanen K, Grenman S, Syrjänen S (2012) Oral Mucosa as a Reservoir of Human Papillomavirus: Point Prevalence, Genotype Distribution, and Incident Infections Among Males in a 7-year Prospective Study. Eur urol 62: 1063-1070.
Costa MC, Bornhausen Demarch E, Azulay DR, Périssé AR, Dias MF, et al. (2010) Sexually transmitted diseases during pregnancy: a synthesis of particularities. An Bras Dermatol 85: 767-782.
Murta E, Souza M, Adad S, Júnior E (2001) Human Papillomavirus Infection in Adolescents: Relation to Contraceptive Method, Pregnancy, Smoking, and Cytologic Findings. Rev Bras Ginecol Obs 23: 217-221.
Brown DR, Shew ML, Qadadri B, Neptune N, Vargas M, et al. (2005) A Longitudinal Study of Genital Human Papillomavirus Infection in a Cohort of Closely Followed Adolescent Women. J Infect Dis 4620: 182-192.
Armbruster-Moraes E, Ioshimoto LM, Leao E, Zugaib M (2000) Prevalence of 'high risk' human papillomavirus in the lower genital tract of Brazilian gravidas. Int J Gynaecol Obstet 69: 223-227.
Hernandez-Giron C, Smith JS, Lorincz A, Lazcano E, Hernandez-Avila M, et al. (2005) High-risk Human Papillomavirus detection and related risk factors among pregnant and nonpregnant women in Mexico. Sex Transm Dis 32: 613-618.
Banura C, Franceschi S, Doorn L Van, Arslan A, Kleter B, et al. (2008) Prevalence , incidence and clearance of human papillomavirus infection among young primiparous pregnant women in Kampala , Uganda. J Cancer 123: 2180-2187.
Tristao W, Ribeiro RM, Oliveira CA, Betiol JC, Bettini Jde S (2012) Epidemiological study of HPV in oral mucosa through PCR. Braz J Otorhinolaryngol 78: 66-70.
Madinier I, Doglio A, Cagnon L, Lefèbvre JC, Monteil RA (1992) Southern blot detection of human papillomaviruses (HPVs) DNA sequences in gingival tissues. J Periodontol 63: 667-673.
Parra B, Slots J (1996) Detection of human viruses in periodontal pockets using polymerase chain reaction. J Microbiol Immunol 5: 289-293.
Bustos DA, Grenon MS, Benitez M, Boccardo G De, Pavan JV (2001) Human Papillomavirus Infection in Cyclosporin-Induced Gingival Overgrowth in Renal Allograft Recipients. J Periodontol 72: 741-744.
Hormia M, Willberg J, Ruokonen H, Syrjänen S (2005) Marginal periodontium as a potential reservoir of human papillomavirus in oral mucosa. J Periodontol 76: 358-363.
Kellokoski J, Syrjanen S, Kataja V, Yliskoski M, Syrjänen K (1990) Acetowhite staining and its significance in diagnosis of oral mucosal lesions in women with genital HPV infections. J Oral Pathol Med 19: 278-283.
Loe H, Silness J (1963) periodontal disease in pregnancy. I. prevalence and severity. Acta Odontol Scand. 21: 533-551.
Akalin, FA, Baltacioglu E, Alver A, Karabulut E (2009) Total antioxidant capacity and superoxide dismutase activity levels in serum and gingival crevicular fluid in pregnant women with chronic periodontitis. J periodontal 80: 457-467.
Armitage GC (1999) Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4: 1-6.
Cavalcanti EF, Silva CR, Ferreira DC, Ferreira MV, Vanderborght PR, et al. (2016) Detection of human papillomavirus in dental biofilm and the uterine cervix of a pregnant adolescent. Sao Paulo Med J 134: 88-91.
Nielsen A, Kjaer SK, Munk C, Iftner T (2008) Type-specific HPV infection and multiple HPV types: prevalence and risk factor profile in nearly 12,000 younger and older Danish women. Sex Transm Dis 35: 276-282.
Kero K, Rautava J, Syrjänen K, Grenman S, Syrjänen S (2011) Human papillomavirus genotypes in male genitalia and their concordance among pregnant spouses participating in the Finnish Family HPV study. J Sex Med 8: 2522-2531.
Loomis DM, Pastore PA, Rejman K, Gutierrez KL, Bethea B (2009) Cervical cytology in vulnerable pregnant women. J Am Acad Nurse Pract 21: 287-294.
Moscicki A, Shiboki S, Broering J, Powell K, Clayton L, et al. (1998) The natural history of human papillomavirus infection as measured by repeated DNA testing in adolescent and young women. J Pediatr. 132: 277-284.
Kumar PS (2013) Sex and the subgingival microbiome: do female sex steroids affect periodontal bacteria? Periodontol 2000 61: 103-124.
Horewicz VV, Feres M, Rapp GE, Yasuda V, Cury PR (2010) Human papillomavirus-16 prevalence in gingival tissue and its association with periodontal destruction: a case-control study. J Periodontol 81: 562-568.
Escalona L, Correnti M, Veitía D, Perrone M (2011) Detection of human papillomavirus in gingival fluid of Venezuelan HIV patients with periodontal disease. Invest Clin 52: 207-215.