This work describes one of the first studies in a Mexican population that evaluates HPV type-specific concordance among heterosexual couples in a rural area in central Mexico. Of 138 couples where at least one partner was infected, approximately 25% (34/138 = 24.6) of the respective partners were simultaneously infected by HPV. Among these couples, type-specific concordance was high (61.8%). The principal predictors of HPV in men were factors related to high-risk sexual behavior. The presence of HPV in both men and women was strongly associated with the detection of HPV in their respective partners.
Studies over the past 20 years evaluating HPV infection concordance among heterosexual partners have shown many inconsistencies, reporting concordances of type-specific infection of between 2 and 87%[5, 6, 8, 16–21]. Such heterogeneous findings may be due to the use of diverse laboratory HPV DNA detection techniques, the methods used to select the study population, and to the anatomical site being sampled (particularly in men), among other factors.
An early report on HPV concordance in heterosexual partners documented that 75% of women whose male partners had HPV were also HPV positive, while only 39% of men with HPV-positive female partners were HPV positive in semen. Female partners of men with condylomatosis of the penis have also been studied, where high-risk cervical HPV has been calculated to be 27.7% and cytologic anomalies in the cervix has been estimated to be 36%. The main limitation of previous studies was primarily methodological. Technological developments over the years in the area of diagnostic testing have led to more sensitive HPV DNA detection tests. Furthermore, the identification of male anatomical regions where HPV is routinely detected has recently been well studied. Therefore, comparisons between population studies are greatly limited due to differences in the methods employed.
Other studies have recently shown concordance findings to be similar to those found in this study; 76% of male partners of infected women have been shown to be HPV positive. Three other studies evaluating type-specific concordance in heterosexual partners reported concordance estimates of 43% a 64.4%, although the sample size was quite small[8, 19, 24]. These results are consistent with the hypothesis of sexual transmission[25, 26] of HPV infections.
An association between the presence of lesions in the sexual partner and the presence of HPV infection was not demonstrated in the current study as the large proportion of infections in this population was subclinical. It is possible that the combined sampling of sites of the scrotum and penile shaft, balano-preputial lamina and urinary meatus has increased the type-specific concordance value found in this study. It has been shown in a previous study that use of combined samples increases HPV DNA detection.
The 13.7% prevalence of HPV infection found in women is less than the prevalence of 20.4% found in men; this lower prevalence in women compared to their male partners has been observed in other studies that evaluate both men and women. The natural history of HPV infection may be different between men and women due to differences between the epithelium in the cervical transformation zone and the penis. HPV DNA prevalence has been shown to be as much as two to three times higher in Mexican men than in Mexican women. With respect to women, HPV prevalence in Mexico has been reported as ranging from as little as 3.7% to as high as 48.9%[28–33] and a systematic review conducted in the United States that includes studies of prevalence in Hispanic, African-American, Asian, Caucasian and other women report prevalences between 14% and 90%. Higher HPV prevalence estimates have been observed among women with high-risk sexual behavior as compared to predominantly monogamous women. This is consistent with prevalence estimates derived from a population-based study of Mexican women and those from a study of women with social security health care services[30, 32]. In addition, prevalence estimates in urban areas, where HPV is endemic, are greater than those observed among women in rural areas and than those observed in countries with a low incidence of and mortality from cervical cancer. The bimodal pattern for HPV infection by age group observed in previous studies of populations with elevated mortality due to cervical cancer[28, 37] was not observed in this study of rural women, showing an elevated prevalence of more than 14% in women older than 30 years, which was consistent up to 75 years of age, the maximum age included.
The above is a reflection of the fact that HPV prevalence of and concordance among couples is not only highly variable but also depends on the sexual behavior of the couples, the sensitivity of the tests employed, and more importantly on the differences between acquisition rates among men and women.
The identification of risk factors associated with HPV detection in our study in both men and women is consistent with that of other reports[38–48]. In men, being single and having fewer years of schooling are associated with an increased risk for HPV infection, as is being younger on sexual debut, having multiple sexual partners, and a history of having had sexual relations with prostitutes. This pattern of risk factors for penile HPV infection is similar to that found in an HPV study among Mexican soldiers. For women, being single and smoking are factors clearly correlated with high-risk sexual conducts and are therefore positively associated with HPV infection, a finding that is also consistent with reports from previous studies[32, 37]. In the present study, we show for Mexican men that a history of sexual relations with sex workers and inadequate use of condoms when having such sexual relations increase the risk of HPV infection in their female partners, indicating, as in many other studies, the key role of the male factor in the risk of HPV infection in the female partner.
The results of this study of couples are singularly important, in part, because this is one of the first studies to quantify type-specific HPV concordance for a female population with a pattern of sexual conduct that is predominantly monogamous. In addition, because HPV prevalence estimates in the external male genitalia was found to be two times higher than that previously reported for Mexican men with low-risk sexual behavior. These findings are bolstered by an external quality control mechanism for the determination of HPV DNA in the study population that included a determination of HPV blind to knowledge of gender and of the HPV results of the corresponding partner. Therefore, information bias with regard to the characterization of the presence of HPV DNA is improbable.
Prospective cohort studies among different populations are warranted to confirm these estimates as well as to quantify the probability of HPV transmission patterns in men and women and explore the role of potentially associated cofactors.