Hpv Positive Then Negative for Years Then Positive Again
Asian Pac J Cancer Prev. 2021 Jun; 22(6): 1907–1912.
Repeated Positive Cervical HPV Testing and Absent or Minor Cytology Abnormality at Pap Smear. What is the Next Step?
Vitor Caeiro
1 Health Sciences Research Centre (CICS), Faculty of Health Sciences, Academy of Beira Interior (UBI), Covilha, Portugal.
Sara Nunes
2 Polytechnic Found of Castelo Branco, Castelo Branco, Portugal.
Bruno Esteves
three Clinical Pathology at Cova da Beira University Hospital Eye (CHUCB), Covilhã, Portugal.
José Fonseca-Moutinho
4 Wellness Sciences Research Centre (CICS), Kinesthesia of Health Sciences, University of Beira Interior (UBI), Covilhã, Portugal.
Received 2021 Mar 15; Accustomed 2021 Jun 22.
Abstruse
Background:
Human papillomavirus (HPV) screening has significantly reduced cervical cancer (CC) mortality. Women who consecutively test positive for high-risk HPV without and minor changes on reflex cytology (singular squamous cells of undetermined significance [ASC-The states] or low-grade squamous intraepithelial lesion [LSIL]) or dysplasia on cervical colposcopy-oriented biopsy are always referred to colposcopy. The aim of the present written report was to assess whether this guidance is appropriate for COBAS HPV testing with reflex cytology.
Methods:
A cross-sectional, retrospective study was carried out in 5,227 women who underwent routine CC screening over a period of five years (2012-2017). All HPV tests were performed using Cobas®4800 HPV. The study included women attention gynecology appointments whose outset HPV test was positive and who had any type of follow-up. Patients' HPV test results as well as cytology and biopsy findings obtained during the abovementioned menstruation were analyzed. A descriptive and comparative statistical report was conducted using this data.
Results:
A total of 765 out of 6003 HPV tests performed in 5,227 women were positive, and 141 women who had a positive HPV examination (with negative for intraepithelial lesion or malignancy [NILM] or inflammation, or ASC-The states and LSIL cytology, simply no lesions on colposcopy, or absence of dysplasia on histology) repeated the HPV test at least once. Of these 141 women, 6 were diagnosed with loftier-grade squamous intraepithelial lesion (HSIL) during the follow-up period. All cases of HSIL were diagnosed subsequently the 2d HPV test.
Conclusion:
This study shows that, at cervical cancer screening, all women testing positive for HPV regardless of Pap smear result should be referred to colposcopy.
Key Words: Cervical cancer, HPV testing, cervical cancer screening, HSIL, CIN
Introduction
Co-ordinate to the World Health System (WHO) statistics, around 15 to xx% of the diagnosed cancers are associated with viral infections. Human papillomavirus (HPV) is one of the viruses contributing to these statistics, increasing the risk of cervical cancer (CC) progression when high-adventure HPV infection persists (Chan et al., 2019). CC is the 4th almost mutual cancer in women worldwide, after breast cancer, colorectal cancer and lung cancer (Bhatla and Denny, 2018).
Screening programs which incorporate HPV testing have consistently been associated with a reduction in CC incidence, potentially decreasing morbidity and mortality (Chan et al., 2019). All the same, CC remains a major public wellness problem, with estimated 569,847 new cases and 311,365 deaths worldwide in 2018 (Bray et al., 2018).
Persistent infection with high-risk HPV genotypes is a necessary but not sufficient condition for disease progression and is the principal epidemiological commuter of loftier-course intraepithelial lesions (HSIL) and invasive carcinoma (Oliveira et al., 2013). HPV infection is subclinical in most cases, peculiarly in younger women where in more fourscore% of cases the infection resolves spontaneously inside 1 to two years. However, approximately 10% of HPV infections can become persistent and about 3 to 4% progress to intraepithelial lesions. Of these, 0.7 to 1% may advance to high-class lesions (CIN 2/iii), existence estimated that 0.ane% will progress to invasive cancer if non detected and treated in a timely way (WHO, 2012).
The natural course of CC is well known, and its carcinogenesis process is slow. The presence of CC forerunner lesions, the availability of sensitive screening tests for detection and effective treatment methods take enabled highly effective secondary prevention, using screening programs (Tsikouras et al., 2016).
The most common CC screening methods are conventional cytology, liquid-based cytology and HPV testing, or an association of the latter two (WHO, 2012). The "standard" screening method has been morphological cytology. Several studies accept shown that HPV testing is more sensitive than cytology lone in detecting and preventing high-grade lesions and progression to cancer. In addition, when using HPV testing equally a screening method, the presence of a negative test allows the screening interval to be extended to 5 years, improving compliance with screening programs and enabling effective cost reductions of approximately 20% (Schiffman et al., 2011; Agorastos et al., 2015; Goodman, 2015; Tsikouras et al., 2016).
In 2017, a national organized CC HPV-based screening program was implemented in Portugal for women betwixt the ages of 25 and threescore years, performed every v years, with reflex cytology for high-risk HPV genotypes other than HPV 16 and 18. This screening plan introduces updates to the previous regional cervical cancer screening programs and states that women with a positive HPV test for genotypes other than 16 and 18 with negative for intraepithelial lesion or malignancy (NILM) cytology should repeat the HPV test within the following year. In case of a 2d HPV examination is positive, the adult female will exist referred for colposcopy. Following 2013 Kaiser Permanent Northern California (KPNC) study results, women with a repetitive positive HPV test with without or minor cytological abnormality (ASC-US/LSIL) and no dysplasia on cervical oriented-colposcopy biopsy should exist recommended to colposcopy based on co-testing and Hybrid Capture 2 (HC2; Qliagen, Germantown, MD) for HPV testing (Katki et al., 2013). However, no scientific report showed whether this approach is useful on cervical cancer screenings based on primary new molecular technologies for HPV testing with reflex cytology.
Our goal was to utilise the opportunistic CC screening programme of the Cova da Beira Academy Hospital Eye (CHUCB), based on primary COBAS HPV testing and triage cytology, to validate colposcopy recommendation for those women with repeated positive HPV exam for genotypes other than HPV sixteen and 18 and NILM or pocket-size lesions on previous cytology and no previous dysplasia detected on cervical oriented-colposcopy biopsy.
Materials and Methods
A cross-sectional and retrospective written report was carried out based on data from the routine CC screening protocol in forcefulness at CHUCB between August 2012 and August 2017. The screening protocol was based on HPV testing as the primary method for all women over 25 years old with no history of CC screening in the past two years who attend gynecology appointments at the CHUCB.
The screening method was the Cobas®4800 HPV test, which detects HPV 16, HPV 18 and other types of HPV (31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66, 68), using the liquid medium Surepath®.
All HPV tests were performed at the Laboratory of the Clinical Pathology Department of the CHUCB, while the cytological and histological tests were conducted at the Anatomical Pathology Department of the CHUCB.
The CC screening program of the CHUCB was designed and implemented by the CHUCB Colposcopy Unit of measurement, where all colposcopic examination were performed. According to the CHUCB screening algorithm, shown in Figure 1, a negative HPV tests should be repeated after three years; a positive HPV test for genotypes 16 or 18 is followed by reflex cytology and referral for a colposcopy; a positive HPV test for other types of HPV is followed by reflex cytology, and if reflex cytology shows NILM, the exam must be repeated after i year; whatsoever other cytological finding requires referral for a colposcopy. After a 2d sequent positive HPV test, the woman is monitored at the Colposcopy Unit of measurement for at least 3 years, regardless of subsequent HPV exam results and cytology findings.
Flowchart of Cervical Cancer Screening Implemented on Cova da Beira University Infirmary Centre (CHUCB). A negative HPV test should exist repeated later 3 years. Nonetheless, women with HPV positive test for other strains than 16 or 18 are examined by reflex cytology. In example of negative for intraepithelial lesion or malignancy (NLIM), cytology should exist repeated afterward ane twelvemonth. Otherwise, women should be referred to colposcopy. In case of infection by HPV 16 or 18 genotypes, the follow-upwards incorporates both cytology and colposcopy
Of all 6,003 HPV tests performed in 5,227 women who underwent routine screening at the CHUCB over the abovementioned five years, 765 (14.6%) women who had a positive HPV test were selected for our study. Of these, we evaluated 141 women who had no history of treatment for cervical intraepithelial neoplasia and had satisfactory cytology findings, classified every bit NILM or minor cytological lesions (ASC-US/LSIL), normal colposcopy and/or no dysplasia on biopsy, and who had follow-upwardly appointments at the Colposcopy Unit of the CHUCB. A biopsy was required during a colposcopy engagement only in the presence of grade 1 or 2 colposcopic findings or signs of invasion. If the transformation zone is classified as type 3 (squamouscolumnar junction not fully visible), endocervical curettage is performed routinely.
A descriptive statistical analysis of the information was performed, using the IBM SPSS awarding software, version 26 (SPSS Inc., Chicago, IL). In all cases, nosotros analyzed the patient'due south age, HPV test results (blazon 16, xviii and others), and cytology and histology findings of the biopsy obtained using colposcopy.
Results
The study sample consisted of 141 women who had a positive HPV examination (to HPV 16, 18 and others) with reflex cytology classified as NILM or modest cytological lesions (ASC-U.s./LSIL), but normal colposcopy and/or no dysplasia on biopsy and who underwent follow-upwards (Table 1). This corresponds to xviii.4% of all women with a positive HPV test during the study, aged between 17 and 69, with a mean age of 39.3 years (standard difference=xi.1). For these women, the mean follow-upward was 36.6 months (standard departure=xviii.5).
Table 1
Sequency of Results Man Papillomavirus (HPV) Tests, Cytology and Histology Results. Data is presented every bit number (percent, %).
| onest Test (northward=141) | 2nd Test (n=141) | threerd Test (north=55) | ivth Test (n=xix) | 5th Test (n=half dozen) | |
|---|---|---|---|---|---|
| HPV test | |||||
| Negative | - | 61 (43.three) | 20 (36.iv) | iv (21.1) | 3 (fifty) |
| HPV xvi | 16 (11.3) | six (4.2) | 2 (3.6) | 1 (5.3) | ane (xvi.6) |
| HPV 18 | 5 (3.five) | - | 1 (i.8) | - | - |
| Others | 102 (72) | 59 (41.8) | 26 (47.3) | xi (57.9) | 2 (33.4) |
| HPV sixteen+others | fifteen (10.6) | 11 (7.viii) | 5 (9.1) | 2 (x.6) | - |
| HPV 18+others | 3 (2.i) | 3 (2.one) | ane (1.eight) | one (5.3) | - |
| CYTOLOGY | |||||
| Non performed | ane (0.7) | 55(39) | 17(31) | ane(five.three) | 3(50) |
| NILM | 101 (71.7) | 51 (36.2) | 28 (fifty.9) | 13 (68.iv) | 2 (33.3) |
| LSIL | 24 (17.0) | 13 (9.3) | iii (5.4) | two (10.five) | - |
| ASC-US | 15 (10.half-dozen) | 15 (ten.6) | 6 (x.9) | 2 (10.5) | one (16.7) |
| HSIL | - | 3 (two.1) | 1 (i.eight) | 1 (5.3) | - |
| ASC-H | - | 4 (2.viii) | - | - | - |
| HISTOLOGY | |||||
| Not performed | 24 (53.three) | 104 (73.7) | 49 (89.i) | xiv (73.vii) | four (66.6) |
| No dysplasia | 21 (46.7) | 18 (12.viii) | 4 (7.three) | 3 (xv.8) | ane (sixteen.7) |
| LSIL | - | xiii (9.ii) | 2 (iii.half dozen) | ii (10.five) | 1 (16.7) |
| HSIL | - | 6 (4.three) | - | - | - |
ASC-H, atypical squamous cells; ASC-US, atypical squamous cells of undetermined significance; HPV, homo papillomavirus; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-form squamous intraepithelial lesion; NILM, negative for intraepithelial lesion or malignancy.
During follow-upwardly, CIN2+ lesions were detected in six (4.3%) women, with a mean age of 35.7 years (standard deviation= vii.7), and all CIN2+ lesions were diagnosed after the second HPV test. No women were diagnosed with invasive carcinoma. The hateful time to diagnosis of CIN2+ lesions was 18.5 months (standard deviation=4.two). The HPV examination, cervical cytology and biopsy results are shown in Table one. Regression charge per unit of HPV infection in the studied group was always very high, especially for types 16 and eighteen, which highlights the transient nature of those HPV infections. Notwithstanding, the multiple infection rate (HPV 16 or eighteen and others) remained unchanged, possibly due to reinfection. Following the starting time test, simply 45 women underwent colposcopy due to a positive HPV 16 or eighteen test and/or ASC-US or LSIL cytology. All women underwent colposcopy in their 2nd, third, fourth and 5th HPV tests. Six women were co-tested for their 2nd HPV test, and 3 women were co-tested for their third and fourth tests.
Table two shows that the prevalence and spontaneous resolution of high-gamble HPV infection was more common in women under thirty years of historic period, while the cytological and histological diagnosis was more serious in the group of women over 30 years of age.
Table 2
Sequency of Human Papillomavirus (HPV) Tests, Cytology and Histology Results Comparing Women under and over 30 Years of Age. Data is presented as number (percentage, %).
| anest Test | twond Test | threerd Test | fourth Examination | 5th Test | ||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Historic period | <30 | >30 | <thirty | >30 | <30 | >30 | <xxx | >30 | <thirty | >30 |
| Number of cases | xxx (21.three) | 111 (78.7) | xxx (21.iii) | 111 (78.7) | 11 (20) | 44 (80) | 2 (1.ane) | 17 (98.9) | - | half-dozen (100) |
| HPV TEST | ||||||||||
| Negative | - | - | fifteen (fifty) | 46 (41.four) | four (36.four) | sixteen (36.3) | 1 (50) | three (17.6) | - | 3 (fifty) |
| HPV 16 | 8 (26.7) | 8 (7.ii) | 1 (3.3) | v (4.v) | 1 (9.ane) | 1 (2.3) | - | 1 (5.ix) | - | 1 (16.7) |
| HPV xviii | - | 5 (four.5) | - | - | one (9.1) | - | - | - | - | - |
| Others | xix (63.3) | 83 (74.8) | 9 (30) | fifty (45) | 5 (45.4) | 21 (47.7) | one (50) | ten (58.8) | - | ii (33.iii) |
| HPV xvi+HPV xviii | - | - | - | 1 (0.9) | - | - | - | - | - | - |
| HPV xvi+others | 3 (10) | 12 (10.i) | 4 (xiii.3) | 7 (half dozen.3) | - | 5 (eleven.four) | - | 2 (11.8) | - | - |
| HPV eighteen+others | - | 3 (2.vii) | 1 (three.three) | 2 (1.8) | - | i (two.3) | - | 1 (5.9) | - | - |
| CYTOLOGY | ||||||||||
| Not performed | 1 (iii.iii) | - | 14 (46.7) | 41 (37) | 3 (27.3) | xiv (31.eight) | 1 (50) | - | - | 3 (50) |
| NILM | twenty (66.7) | 81 (73) | 12 (40) | 39 (35 | viii (72.vii) | xx (45.5) | 1 (50) | 12 (70.half-dozen) | - | 2 (33.3) |
| LSIL | 6 (20) | xviii (xvi.2) | 2 (half-dozen.7) | 11 (x) | - | 3 (six.8) | - | ii (eleven.viii) | - | - |
| ASC-U.s.a. | 3 (10) | 12 (10.eight) | 1 (three.3) | 14 (12.vi) | - | 6 (thirteen.vi) | - | 2 (11.8) | - | 1 (16.7) |
| HSIL | - | - | 1 (3.three) | 2 (1.viii) | - | 1 (2.three) | - | 1 (v.viii) | - | - |
| ASC-H | - | - | - | 4 (three.six) | - | - | - | - | - | - |
| HISTOLOGY | ||||||||||
| Not performed | 6 (twenty) | 18 (16.2) | 24 (fourscore) | 80 (72) | ix (81.8) | 40 (91) | one (50) | 12 (70.6) | - | 4 (66.half-dozen) |
| No dysplasia | 3 (10) | xviii (sixteen.2) | 2 (6.7) | xiv (12.half dozen) | 2 (18.ii) | ii (4.5) | 1 (50) | 3 (17.6) | - | 1 (xvi.seven) |
| LSIL | - | - | - | 13 (eleven.vii) | - | 2 (4.5) | - | 2 (xi.8) | - | i (sixteen.vii) |
| HSIL | - | - | two (6.7) | 4 (3.half-dozen) | - | - | - | - | - | - |
ASC-H, atypical squamous cells; ASC-United states of america, atypical squamous cells of undetermined significance; HPV, man papillomavirus; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion; NILM, negative for intraepithelial lesion or malignancy.
Table 3 shows the relevant aspects of the 6 cases where HSIL was diagnosed during patient follow-up. Iv of these 6 cases were diagnosed in women anile thirty or over. HSIL was associated with HPV xvi infection in only ane woman, and cytology had been classified as NILM or ASC-U.s. or LSIL in 4 women.
Table iii
Detailed Description of Loftier-Form Squamous Intraepithelial Lesion (Cases of HSIL) Diagnosed during Written report Follow-up
| Description of positive cases | ||||||
|---|---|---|---|---|---|---|
| Age | anest HPV Examination | onest Cytology | twond HPV Exam | iind Cytology | Fourth dimension to diagnosis | Notes |
| 25 years old | xvi + Others | NILM | Others | HSIL | xviii months | |
| 27 years old | 16 + Others | LSIL | 16 + Others | LSIL | 22 months | 1) |
| xxx years quondam | Others | NILM | Others | HSIL | 25 months | |
| 40 years former | Others | NILM | Others | NILM | sixteen months | 2) |
| 42 years quondam | Others | LSIL | Others | ASC-United states | 14 months | |
| 50 years old | Others | LSIL | Negative | ASC-United states | xvi months | 3) |
ASC-US, singular squamous cells of undetermined significance; HPV, human papillomavirus; HSIL, loftier-class squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion; NILM, negative for intraepithelial lesion or malignancy; one) Despite LSIL cytology, the patient underwent colposcopy and biopsy revealing HSIL; 2) Despite NILM cytology, the patient underwent colposcopy and biopsy revealing HSIL; three) Co-testing (HPV testing + cytology) Patient underwent colposcopy and biopsy revealing HSIL
Give-and-take
The protocol used in this study was the CC screening protocol of the Gynecology Department of the CHUCB, which recommends HPV testing as the primary test in routine screening. This is an institutional screening program which, among other aspects, is open to all patients attention gynecology appointments (including significant women) and had the participation of all physicians who offer gynecology appointments at the CHUCB. This cervical cancer screening was implemented at the CHUCB to manage patients and to mitigate the effects of low compliance with the national screening program.
The CC screening protocol at the Gynecology Section of the CHUCB starting time at 2012 was organized following 2011 ATHENA HPV study results (Wright et al., 2012).
A high pct of women under the age of 30 were included in the study population. The CC screening protocol in force at the CHUCB includes women over 25 years of age and some physicians did not comply with the inclusion criteria. There was a higher prevalence and spontaneous resolution of high-gamble HPV infection in the group of women under thirty years of historic period, as well every bit less serious cytological and histological diagnoses, which is in accordance with the literature.
The HPV test used for screening was the Cobas®4800 HPV test, which is a qualitative test that uses real-time PCR engineering science to simultaneously detect DNA from 12 types of man recombinant HPV (31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66, and 68) and individually detect HPV xvi and 18. β-globin gene is amplified as an internal control. It can be used equally a main screening method with reflex cytology for positive HPV or in add-on to cytology (co-testing). Thus, CIN3+ take chances stratification is improved, increasing sensitivity for early detection of cervical cancer, with a negative predictive value very close to 100% (Chan et al., 2019).
The liquid medium used for transport and preservation of all samples for cytology was SurePath®, which does non exhibit meaning differences in terms of cutting-off values, when compared to other certified liquid collection media, for the detection of CIN1, CIN2+ and CC lesions (Rozemeijer et al., 2016).
Some women who had a positive HPV test did non undergo follow-up because they had a surgery for a benign condition (uterine fibroids or pelvic organ prolapse corrections), or they stopped attending appointments.
In accordance with literature, the pct of multiple infections was different according to age, suggesting transient reinfection rather than a persistent infection (Pista et al., 2011).
From the assay of the 6 cases of HSIL diagnosed, we highlight the importance of performing colposcopy later the 2d test, as all our cases were diagnosed at this time. Our results are validated by other studies reporting similar situations (Melnikow et al., 2018; Gu et al., 2019). The second cytology was suggestive of HSIL in only two cases, and it was classified equally NILM in ane example, which reinforces the value of colposcopy in these situations.
The absenteeism of HSIL diagnosed afterwards the second HPV examination is probably due to the referral for colposcopy of all patients afterwards the second positive HPV exam, regardless of cytology findings. This procedure allowed HSIL identification which was not diagnosed during the first test. Between the kickoff and 2d tests, it is more likely that there was regression than progression of dysplastic lesions, which may also explicate in function why no other cases of HSIL were diagnosed after the second test. The outcome of any HPV-based CC screening is highly dependent on the number of lesions detected using colposcopy-directed biopsy, which reinforces the importance of quality colposcopy practices. Avoiding unnecessary biopsies without neglecting the diagnosis of cervical cancer forerunner lesions is of paramount importance, and all women with positive HPV tests should be referred to different colposcopy units, as was the case in this study.
This study demonstrates that women undergoing HPV-based CC screening who had one positive HPV test with NILM, ASC-US or LSIL cytology, with normal colposcopic findings and/or no dysplasia on cervical biopsy, should be referred for colposcopy in the presence of a second positive HPV test, regardless of the cytology findings. This procedure is standardized in the electric current cervical cancer screening programme in Portugal and recommended by 2019 American Society for Colposcopy and Cervical Pathology (ASCCP) guidelines (Perkins et al., 2020).
This written report has some limitations. The CC screening method used at the CHUCB is an institutional routine programme based on a random population that attends gynecology appointments and includes meaning women, and it is non an organized screening plan. Furthermore, sample size is express as the geographic localization of CHUCB only serves a population of approximately ninety,000 people which includes the municipalities of Covilhã, Fundão, Belmonte and Penamacor. Only women referred by CHUCB physicians to the CHUCB Colposcopy Unit were evaluated in this study. Many of these women had previously participated in the organized cervical cancer-screening program in the Centre Region of Portugal, which has been in place for more than 20 years. The influence of HPV vaccination on the results was not evaluated because the pct of vaccinated women was small at the time of data collection.
Notwithstanding, the results of our study concerning HPV and cytology abnormalities prevalence are in understanding with studies performed in other countries, such as the HEllenic Real life Multicentric cErvical Screening study group, in Greece (HERMES) (Agorastos et al., 2015) and a study that evaluates the efficacy outcomes of main HPV testing based on the follow-up of randomized controlled trials in Germany (WOLPHSCREEN), Sweden (SWEDESCREEN), England (ARTISTIC), holland (POBASCAM) and Italy (NTCC) (Ronco et al., 2014). Therefore, we tin can conclude that our studied population was adequate for valid conclusions. In add-on, our report is in agreement with recent published 2019 ASCCP Risk-Based Direction Consensus Guidelines for Abnormal Cervical Cancer Screening Tests and Cancer Precursors (Perkins et al., 2020), that recommend colposcopies for all women with repeated positive HPV testing with NILM or pocket-sized cytology abnormalities.
This report has shown that, regardless of reflex cytology findings, women who have at to the lowest degree 2 sequent positive cervical HPV tests are at increased gamble of having previously undiagnosed cervical HSIL and should always be referred for colposcopy. Additionally, the chance of intraepithelial lesions or malignancy was independent of the type of HPV adamant. All women with cervical repeated positive HPV testing and with absent or pocket-sized cytology abnormalities should exist referred to colposcopy in an independent manner of screening adopted program and engineering used for HPV testing, as recommended past ASCCP.
Abbreviations
ASCCP – American Society for Colposcopy and Cervical Pathology; ASC-H – atypical squamous cells; ASC-U.s.a. – atypical squamous cells of undetermined significance; CC – cervical cancer; CHUCB – Cova da Beira Academy Hospital Center; CIN – cervical intraepithelial neoplasia; Co-testing: Concomitant HPV test and cytology; HPV – human being papillomavirus; HSIL – high-grade squamous intraepithelial lesion; KPNC – Kaiser Permanent Northern California; LSIL – low-grade squamous intraepithelial lesion; NILM – negative for intraepithelial lesion or malignancy; SPSS – Statistical Parcel for the Social Sciences.
Author Contribution Statement
Vitor Caeiro: Conducted the investigation and write manuscript; Sara Nunes: Organize statistical analysis of data and review the manuscript; Bruno Esteves: Responsible by HPV testing and pap smear and review the manuscript; José Fonseca-Moutinho; Advisor and review the manuscript.
Acknowledgments
The writer would like to give thanks CHUCB for providing the facilities for this report. This research did not receive whatsoever specific grant from funding agencies in the public, commercial, or not-for-profit sectors. This work is part of Vitor Caeiro doctoral program.
Conflict of interest
The authors take no conflict of interest to declare. This research was approved Ethics Commission of Beira Interior University with the code CE-UBI-Pj-2017-027.
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