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Sexually Transmitted Diseases:
doi: 10.1097/OLQ.0b013e3181feae89
Original Study

Human Papillomavirus Incidence and Risk Factors Among Mexican Female College Students

Sánchez-Alemán, Miguel A. DSc*; Uribe-Salas, Felipe J. DSc†; Lazcano-Ponce, Eduardo C. DSc‡; Conde-Glez, Carlos J. PhD*

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From the *Centro de Investigaciones sobre Enfermedades Infecciosas, Instituto Nacional de Salud Pública, Cuernavaca, Morelos, México; †Colegio de la Frontera Norte, Piedras Negras, Coahuila, México; and ‡Centro de Investigación en Salud Poblacional, Instituto Nacional de Salud Pública, Cuernavaca, Morelos, México

Correspondence: Carlos J. Conde-Glez, PhD, Centro de Investigaciones sobre Enfermedades Infecciosas, Instituto Nacional de Salud Pública, Avenida Universidad 655, Colonia Santa María Ahuacatitlán, CP 62100, Cuernavaca, Morelos, México. E-mail: cjconde@insp.mx.

Received for publication April 26, 2010, and accepted September 8, 2010.

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Abstract

Objective: To determine the factors associated with high-risk human papillomavirus (HR-HPV) and its incidence in a cohort of female college students, with particular emphasis on the use of condoms.

Methods: A cohort was created during 2001 to 2005. The students signed informed consent, answered a questionnaire, and provided a vaginal scrape to detect HR-HPV. Incidences were estimated and risk factors were evaluated using Cox proportional risk model. The variable condom use was constructed based on the following 3 measurements: relative frequency throughout one's lifetime, use during the first sexual relationship, and use during the last sexual relationship.

Results: A total of 237 women participated, providing 395.6 person-years of follow-up. An incidence of 15.9 HR-HPV infection per 100 person-years was estimated and the factors associated with HR-HPV infection were found to be self-reported sexually transmitted infections (RR = 2.7), use of emergency contraception pill (ECP) (RR = 2.0), and having 2 or more sexual partners (RR = 1.9). University students using the ECP demonstrated more risky sexual behavior than nonusers. Women with 2 or more sexual partners who reported inconsistent condom use had 3.8 times the rate of HR-HPV infection.

Conclusions: The incidence for HR-HPV in this cohort of Mexican female college students is comparable to that found in the United States and Canada. The results suggest that the consistent use of condoms is a protective factor against HR-HPV, especially for women with multiple sexual partners and/or those who use the ECP.

Longitudinal studies have shown that alcohol consumption, smoking, marijuana use, and multiple sexual partners1–4 are the risk factors of acquiring human papillomavirus (HPV) among young women; oral contraceptives have provided contradictory results, with findings showing that it is both a risk factor for HPV2 as well as a protective factor3 against the infection. The use of condoms is an important variable for preventing sexually transmitted infections (STIs)5; however, it has not been reported to be a protective factor against acquiring HPV because research has resulted in contradictory findings.6 The “ineffectiveness” of the condom for preventing HPV infection may be due to several causes: (1) risk compensation as a result of men who use the condom, feeling safe and thus having a greater number of sexual partners7; (2) longitudinal studies are the only ones that correctly evaluate the temporal relationship between condom use and HPV, and most of the studies that have been conducted are cross-sectional studies6; (3) measure the use of condom—-frequency (always, almost always, never) and at what moment in time (lifetime condom use, first sexual relationship, and last sexual relationship).8

The present article studied the incidence of high-risk HPV (HR-HPV) and the risk factors associated with acquiring the infection in a cohort of Mexican female college students, with emphasis on the usefulness of the condom as a protective factor.

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METHODOLOGY

The entire female population from schools of Medicine, Psychology, and Pharmacy from Autonomous State University of Morelos was invited to participate in 2001 and newly enrolled students were invited during 2002 and 2003, conforming baseline population. Follow-up of the population was carried out during the years 2002, 2003, and 2005; it was not possible to conduct research in 2004 due to a labor conflict at the institution. Students signed informed consent, answered a self-administered questionnaire about demographic and sexual behavior characteristics, and provided self-collected vaginal scrape samples (Female Swab Specimen Collection Kit, Digene). The detection of HPV was performed using the Hybrid Capture 2 High-Risk HPV DNA test, only among sexually active students. The variable condom use was coded according to the following 2 categories: (1) consistent—always, frequency over one's lifetime, and (2) inconsistent—almost always, half of the time, almost never, never, frequency of use over one's lifetime. Later, the “consistent” stratum was codified to take into account the use of condoms during the first sexual relationship and the last sexual relationship, and if for one of these variables the participant mentioned no condom use, they were reclassified as inconsistent. Use of the emergency contraception pill (ECP) was determined on the basis of the contraceptive method most used by the participants during the past 12 months. Factors such as tobacco and marijuana use, the number of sexual partners, having casual partners, and same sex partners also refer to the past 12 months.

A bivariate analysis was conducted to identify the incidence density for each stratum for the variables analyzed, using person-years (py) of follow-up. Association measurements were calculated using Cox proportional risk model, with person-years of follow-up as the variable for time. Finally, a multivariate saturated model was constructed, adjusting for all statistically significant variables (Wald P value) without casual partners because of collinearity with sexual partners. The statistical analysis was performed with SPSS 15.0.

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RESULTS

The baseline population of the cohort of female college students was 622 women, of which 366 did not receive follow-up and 19 women with follow-up were positive at baseline. The population studied included 237 subjects providing 395.6 py of follow-up, on average, the female college students had 1.71 years of follow-up. The average age at baseline was 21.2 years and the average age at sexual debut was 18.7 years with partners who were 21.6 years of age, on average. Table 1 presents the demographic characteristics and sexual behavior of the 237 women at baseline. Ten percent of students had consumed illegal drugs, 6.8% mentioned using the ECP as their regular method of contraception, and 80% reported that their partner did not always use a condom.

Table 1
Table 1
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In this population, 63 new cases of HR-HPV infection were detected, with an incidence of 15.9 HR-HPV infections (95% confidence interval, 12.3–19.5) per 100 py. Table 2 presents the incidence of HR-HPV infection and Cox proportional risk; participants with a history of STIs had an incidence of 39.8 HR-HPV infections per 100 py. The use of the ECP was associated with a greater incidence of HR-HPV (37.2 vs. 14.5 per 100 py) than non-ECP users. Women with 2 or more sexual partners had 28.8 HR-HPV infections per 100 py, almost twice the rate of acquiring infection than participants with 1 sexual partner. Women who had inconsistent condom use had twice the rate of HR-HPV infection; however, the significance was lost when adjusting the variables.

Table 2
Table 2
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Table 3 shows the variables condom use and ECP use stratified by the number of sexual partners. Women with 2 or more sexual partners who reported inconsistent condom use had 3.8 times the rate of acquiring HR-HPV than women who used condoms consistently and who had 1 sexual partner. Female college students who used the ECP and who had 2 or more sexual partners had higher incidence of HR-HPV infection than women who did not use the ECP and who had 1 sexual partner (45.5 vs. 12.1 per 100 py, respectively).

Table 3
Table 3
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DISCUSSION

The incidence of HR-HPV infection (15.9 per 100 py) among Mexican female college students is similar or slightly less than that observed in studies conducted in other parts of the world, either for all HPV types or in one instance HR-HPV: female university students in the United States (14.3 all HPV,1 16.1 all HPV,2 and 22.2 all HPV9), women seeking contraceptive information in the United States (14.6 all HPV10), and women attending clinics in Canada (16.8 HR-HPV11). HPV is, therefore, a public health problem in the study population that warrants greater attention.

HPV studies have consistently found that the number of sexual partners is a risk factor of HPV infection (4 or more partners in 6 months,1 new partner in the past month,3 and new partner in the past 3 months4). However, although the female college students analyzed presented fewer changes in sexual partners (2 or more in the past year) than the studies mentioned above, they had twice as much risk of acquiring HR-HPV, because an increase in the number of sexual partners increases the possibility of meeting a partner who is infected.

The self-reported history of STIs represented the greatest risk of HPV infection in the cohort analyzed, consistent with the report by Moscicki et al3 that a history of genital warts and HSV-2 represented a greater risk of HPV infection. It is possible that the presence of genital lesions and microlesions makes the mucosa more susceptible to acquiring HPV, in a similar way to that which has been described in the case of Human Immunodeficiency Virus.12 History of STIs in the population studied by the present research may be underestimated because it was not clinically or laboratory confirmed, thus the rate of HR-HPV infection may be even higher because classification errors tend to result in risks decreasing to null.

Another risk factor for HR-HPV infection was the use of the ECP, a hormonal method that can be used as a measurement for nonuse of condoms. In fact, 95.8% of women who used the ECP reported not always using a condom. Female college students who used the ECP were of the same age as nonusers (21.1 ± 1.7 vs. 21.2 ± 2.7, P = 0.946), ECP users had more sexual partners during their lifetime (3.1 ± 2.1 vs. 1.9 ± 1.9, P = 0.003), more partners during the past year (1.8 ± 1.2 vs. 1.3 ± 0.9, P = 0.009), sexual debut at a younger age (17.8 ± 1.4 vs. 18.7 ± 1.8, P = 0.014), and reported having had more relations with casual partners (25.0% vs. 8.1%, P = 0.005) than non-ECP users, this is a subgroup with high-risk sexual behavior.

Although numerous studies have been conducted to measure the effectiveness of the use of condoms to prevent HPV infection (oncogenic and nononcogenic), the results have not been conclusive.6 The usefulness of the condom was evaluated in the United States and showed that university students with 100% condom use presented an incidence of 37.8 HPV infections (all types) per 100 py, whereas those with less than 5% condom use had an incidence of 89.3 HPV infections per 100 py.8 The current study found that when stratifying by the principal risk variable—number of sexual partners—the usefulness of the condom to prevent HR-HPV infection was observed, especially for women with multiple sexual partners. Therefore, the risk of infection apparently can be decreased by the consistent and appropriate use of the condom.

This study had a 50% loss which affected the power of the study, particularly to determine the usefulness of the condom alone to avoid HR-HPV infection. Another possible limiting factor for this work is the issue of self sampling, which could have rendered an underestimation of HR-HPV infection. Without a doubt, it is necessary to continue to study the risk factors for contracting HR-HPV and the incidence of infection in Mexico among diverse populations that include both men and women. The use of more specific biomarkers might also be needed, such as viral load and viral typing, to help increase the knowledge of HPV natural history. In conclusion, this work has identified a subgroup with high-risk sexual behavior, which should be the focus of preventive steps in order to avoid HPV infections and other STIs.

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REFERENCES

1.Ho G, Bierman R, Beardsley L, et al. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998; 338:423–428.

2.Winer RL, Lee S, Hughes JP, et al. Genital human papillomavirus infection: Incidence and risk factors in a cohort of female university students. Am J Epidemiol 2003; 157:218–226.

3.Moscicki AB, Hills N, Shiboski S, et al. Risks for incident human papillomavirus infection and low-grade squamous intraepithelial lesion development in young females. JAMA 2001; 285:2995–3002.

4.Giuliano AR, Harris R, Sedjo RL, et al. Incidence, prevalence, and clearance of type-specific human papillomavirus infections. The young women's health study. J Infect Dis 2002; 186:462–469.

5.Holmes KK, Levine R, Weawer M. Effectiveness of condoms in preventing sexually transmitted infections. Bull World Health Organ 2004; 82:454–461.

6.Manhart LE, Koutsky LA. Do condoms prevent genital HPV infection, external genital warts, or cervical neoplasia? A meta-analysis. Sex Transm Dis 2002; 29:725–735.

7.Steiner ML, Cates W. Condoms and sexually transmitted infections. N Engl J Med 2006; 354:2642–2643.

8.Winer RL, Hughes JP, Feng Q, et al. Condom use and the risk of genital human papillomavirus infection in young women. N Engl J Med 2006; 354:2645–2654.

9.Thomas KK, Hughes JP, Kuypers JM, et al. Concurrent and sequential acquisition of different genital human papillomavirus types. J Infect Dis 2000; 182:1092–1102.

10.Woodman CB, Collins S, Winter H, et al. Natural history of cervical human papillomavirus infection in young women: A longitudinal cohort study. Lancet 2001; 357:1831–1836.

11.Richardson H, Kelsall G, Tellier P, et al. The natural history of type-specific human papillomavirus infections in female university students. Cancer Epidemiol Biomarkers Prev 2003; 12:485–490.

12.Wald A, Link K. Risk of human immunodeficiency virus infection in herpes simplex virus type 2-seropositive persons. A meta-analysis. J Infect Dis 2002; 185:45–52.

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