Prevalence variation of colpocytological abnormalities in adolescents and adults in the years 2000 and 2010

Introduction: Cancer of the cervix is the second most common cancer among women worldwide and the frequency of precancerous lesions is increasing among adolescents. Objective: To study and compare the frequency of epithelial abnormalities in cervical cytology exams in adolescents and adults. Materials and methods: Retrospective study based on analysis of reports of cytology exams performed in the years 2000 and 2010 in adolescents (12-18 years old) and in adult women. The frequency of cytological alterations was explored, stratifying them into high-grade/carcinoma and low-grade lesions. Results: In 2000, rates of epithelial abnormalities were 3.08% in adolescents and 1.39% in adult females, and were 4.76% and 1.83% in 2010, respectively. The high-grade lesions/carcinomas were more common among adults in both years. Discussion: There was an increase in prevalence of epithelial abnormalities in the last decade, both in adolescents and in adults. Proportionally, the increase was higher among adolescents (6.7%) than in adults (2.2%). However, the rate of high-grade lesions/carcinoma was higher among adult women in the two analyzed years. Conclusion: It was observed that the frequency of cervical epithelial abnormalities was higher among adolescents than adults and increased between 2000 and 2010.


intRoDuCtion
Cancer of the cervix is the second most common cancer among women worldwide.Its incidence, of approximately 500 thousand cases per year, is responsible for around 230 thousand annual deaths, with a higher number of reported cases in developing countries.The incidence of cervical cancer begins to rise in the age group of 20-29 years, and the risk increases rapidly to reach a peak, generally in the 45-49 age group, being a rare condition in adolescence (1,2) .
Studies suggest that the frequency of pre-neoplastic lesions has increased among adolescent females.This situation may be justified by the change in behavior patterns of this group, such as the earlier age at first sexual intercourse and the increased number of partners (3,4) .Therefore there is a higher probability of infection by human papillomavirus (HPV), which is the primary risk factor for the development of invasive cervical cancer.Data from the World Health Organization (WHO) estimate that 25%-30% of the women under 25 years of age may be infected with high-risk HPV (2,(5)(6)(7)(8)(9) .
HPV infection is one of the most common sexually-transmitted diseases among young women, with a prevalence that may reach 82% in some populations.Most of these infections are eliminated by the immune system within two or three years, but the persistent ones caused by oncogenic viruses (high risk) have the potential to evolve to invasive carcinoma (10) .
It is known that adolescents with low-risk intraepithelial lesion rarely develop high-grade lesions or carcinoma (2,9,11,12) .Their risk for the development of invasive carcinoma is low, accounting for less than 0.2% of cervical carcinomas, when diagnosed before the age of 20 (10) .In addition, recent guidelines from several organizations, including United States Preventive Service Task Force (USPSTF), American Cancer Society (ACS)/American Society for Colposcopy and Cervical Pathology (ASCCP)/American Society for Clinical Pathology (ASCP) and American College of Obstetricians and Gynecologists (ACOG), recommend that cervical screening begin at age 21 years (13) .

oBjECtivE
The objective of this study was to assess the frequency of epithelial abnormalities in cervical cytology exams of adolescent females in 2000 and 2010, and compare them with equivalent data from the adult population and literature data.

MatERiaLS anD MEthoDS
A cross-sectional retrospective observational study was conducted based on results of cervical cytology tests at Centro de Diagnósticos Anatomopatológicos (Cedap)/Serviços Integrados de Patologia (Sip), in Joinville-SC, which serves public and private hospitals.A total of 94,936 cervical cytology reports were analyzed: 31,078 from 2000 and 63,858 from 2010.The examined reports included conventional and liquid-based cytology tests, stained by Papanicolaou method.Results from patients with previous exams indicating abnormalities were also considered, and those with unsatisfying results were excluded.
The presence of epithelial abnormalities was assessed, including low-grade squamous intraepithelial lesion (LSIL), high-grade squamous intraepithelial lesion (HSIL), carcinoma and adenocarcinoma.These are described according to the criteria defined by Nomenclatura Brasileira para Laudos de Colpocitologia (the Brazilian Nomenclature for Cervical Cytology Reporting) (14) .
Patients aged 12-18 years were considered adolescents, as established by the Brazilian Child and Youth Statute; those aged 19 or over were considered adults.The frequency of cytological alterations of adolescents was compared with that of adult patients and the relationship between them was studied.
The obtained data were retrieved from the proprietary laboratory information system.Proportions were tested by the chisquared method, and the considered level of significance was lower than 0.05.
The research project was approved by the Research Ethics Committee of Hospital Municipal São José, in Joinville-SC (report 161.733 of November 2012).

RESuLtS
Among the 94,936 cytology tests analyzed in 2000 and 2010, 2,132 were from adolescents.In 2000, 31,078 cervical cytology reports were assessed, with 746 from adolescents; 23 were diagnosed with epithelial abnormalities, accounting for 3.08%.In that same year, 30,332 exams of adult patients were recorded, with 422, that is, 1.39%, presenting epithelial abnormalities (Table 1).Among the 63,858 exams assessed in 2010, 1,386 were from adolescents, and 66 of them had diagnosis of epithelial abnormality, what accounts for 4.76%.In the group of adult females, 62,472 exams were recorded, with 1,142 (1.83%) presenting abnormalities (Table 1).
The increased number of adult women with lesions, when comparing both years, is statistically significant.However, the difference between adolescents with lesion when comparing the different years is not statistically significant, in spite of a tendency of increase in the number of cases in this group: from 3.08% to 4.76%.Besides, the percentage difference of epithelial abnormalities between the groups of adolescents and adults is statistically significant, both in 2000 (p < 0.001) and in 2010 (p < 0.001).
Epithelial abnormalities were stratified into two groups.The first included low-grade epithelial lesions; the second, highgrade intraepithelial lesions and carcinomas.Both groups were subdivided by population (adolescents and adults), and by year (2000 and 2010).
In 2000, among the adolescents, 22 results of low-grade intraepithelial lesions and one result of high-grade intraepithelial lesion were recorded.In the same year, among the adults, 308 patients with low-grade intraepithelial lesion and 114 with highgrade intraepithelial lesion or carcinoma were found (Table 2).
In 2010, 65 adolescents with low-grade intraepithelial lesion and only one with high-grade intraepithelial lesion were recorded.In the same year, among adults, 784 results were low-grade intraepithelial lesion and 358 were high-grade intraepithelial lesion or carcinoma (Table 2).
Results did not diverge significantly when both decades were compared.Nonetheless, both in 2000 and in 2010, adult women presented significantly increased prevalence of highgrade lesion or carcinoma, in comparison with the group of adolescents (Table 2).

DiSCuSSion
As observed in the present study, the frequency of cytological epithelial abnormalities in adolescent females is higher than in adult females, what has been reported in the literature (9) .In this study, though, both in 2000 and in 2010, adult women presented a significantly increased prevalence of high-grade lesion or carcinoma in relation to the group of adolescents.Variation in epithelial lesion prevalence among the adolescent population in the last years has not been openly reported.
This study observed an increased prevalence of cervical cytology tests with epithelial abnormalities among adolescents when reports of 2000 and 2010 were compared.Proportionally, there was a 6.7% increase in abnormality rates among adolescents, and just a 2.2% among adult women.
The group of low-grade intraepithelial lesions was the most prevalent in both age groups in both years analyzed in this study.As expected, the group of high-grade lesions was significantly larger in the adult population.
Biomolecular tests for the investigation of the oncogenic HPV type were carried out in 111 adolescents, from 2002 to 2004, in Maceió.A 27% prevalence of positivity was found, with 21.6% of the patients in the age group 15-19 years (15) .In Rio de Janeiro, from 1993 to 2003, an 8.4% prevalence of intraepithelial lesions was found in adolescents, with 3% high-grade lesions, including a case of invasive carcinoma (7) .In Acre, in 2001, a 6.9% rate of cellular epithelial alterations was found in the 15-19 years age group (16) .
The high prevalence of cervical epithelial abnormalities among adolescents, observed in our study and described in the literature, reflects the importance of public policies directed towards primary prevention of sexually-transmitted diseases in that population.
Most women should start cervical/vaginal cancer screening at age 21 years.On the other hand, sexually active adolescents, especially those with immune deficiency, should be screened for precursor lesions as soon as associated factors, such as HIV infection, organ transplantation or long-lasting corticosteroid therapy have been observed (17)(18)(19) .Also, all adolescents should be duly informed about HPV infection and its associated risks.
Bumbulliene et al. (2012), in their study with women aged 15-22, confirmed that smoking, early age at first sexual intercourse, multiple partners and unprotected sex are related to high-risk HPV infection (20) .For this reason, the use of condoms is important for the control of HPV infection and must be recommended to all sexually active adolescents.Besides, vaccination programs may result in a reduction of HPV infections (18,21,22) .Cytology screening, in its turn, has not been indicated for patients under 21 due to the low risk of evolution of low-grade to high-grade lesions, according to literature data and the results achieved in this study.

ConCLuSion
The frequency of abnormalities found in this study is proportionally higher among adolescent than among adult females in the population of Joinville and the region around.A tendency of growth in the frequency of cervical cytological alterations was also observed in adolescents when the beginning of the 2000 decade was compared with the beginning of the 2010 decade.
Considering that HPV is a sexually-transmitted virus, it is evident that the group of adolescents needs attention and care aimed at preventing the transmission of this virus and other sexually-transmitted diseases.At the same time, the low percentage of high-grade lesions in this group revealed by this study strengthens the guidelines about cytology screening in women younger than 21 years, found in the current literature.

taBLE 2 -
Prevalence variation of colpocytological abnormalities in adolescents and adults in the years 2000 and 2010 Classification of epithelial abnormalities detected in cervical cytology tests from adolescent and adult women in 2000 and 2010