Sexually Transmitted Diseases:
Twenty-Year Trends in the Incidence and Prevalence of Diagnosed Anogenital Warts in Canada
Kliewer, Erich V. PHD*†‡; Demers, Alain A. PHD*†; Elliott, Lawrence MD†§; Lotocki, Robert MD|¶; Butler, James R. G. PHD#; Brisson, Marc PHD**
From the *Department of Epidemiology and Cancer Registry, CancerCare Manitoba, Winnipeg, Manitoba, Canada; the †Department of Community Health Sciences, University of Manitoba, Winnipeg, Manitoba, Canada; ‡Cancer Control Research, British Columbia Cancer Agency, Vancouver, British Columbia, Canada; the §Department of Medical Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada; the |Manitoba Cervical Cancer Screening Program, CancerCare Manitoba, Winnipeg, Manitoba, Canada; the ¶Department of Obstetrics, Gynecology, and Reproductive Sciences, University of Manitoba, Winnipeg, Manitoba, Canada; the #Australian Centre for Economic Research on Health, Australian National University, Canberra, Australia; and the **Department of Social and Preventive Medicine, Laval University, Quebec City, Quebec, Canada
The authors thank Manitoba Health for providing the data for this study; and Grace Musto of CancerCare Manitoba for undertaking the computer programming for the analyses.
Supported by an unrestricted Merck Frosst Canada grant to CancerCare Manitoba.
The results and conclusions are those of the authors and no official endorsement by Manitoba Health is intended or should be inferred.
Correspondence: Erich Kliewer, PhD, Cancer Control Research, British Columbia Cancer Agency, 675 West 10th Avenue, Vancouver, British Columbia, V5Z 1L3. E-mail: firstname.lastname@example.org.
Received for publication September 17, 2008, and accepted December 8, 2008.
Supplemental digital content is available for this article. Direct URL citations appear in the printed text, and links to the digital files are provided in the HTML text of this article on the journal’s Web site (http://www.stdjournal.com).
Background: A vaccine has recently been licensed in many countries that protects against the human papillomavirus types 6, 11, 16, and 18. Types 6 and 11 account for approximately 90% of anogenital warts (AGWs). We describe the 20-year trends in the incidence and prevalence of AGWs in Manitoba, Canada.
Methods: We used linked population-based hospital and physician databases for Manitoba for 1984 to 2004. Cases were identified using tariff (billing) and ICD codes. A case was considered to be incident if it was preceded by a 12-month interval free period of AGWs care. Otherwise, it was deemed to be prevalent. An episode was considered over once a 12-month interval had elapsed without an AGW claim.
Results: Approximately 25,000 Manitobans were diagnosed with AGWs between 1985 and 2004. The annual age-standardized incidence rates peaked in 1992 (men, 149.9/100,000; women 170.8/100,000). In recent years, the rates have been increasing again, particularly for men. The male:female incidence rate ratio increased from 0.76 in 1985 to 1.25 in 2004. The highest incidence rate tended to be in those aged 20 to 24 years. Trends in prevalence were similar. Prevalence in 2004 was 165.2/100,000 for men and 128.4/100,000 for women.
Conclusions: These population-based findings suggest that AGWs are a substantial burden to Manitobans and that their pattern has changed over time, with incidence and prevalence becoming higher in men than women. Monitoring the future trends in AGWs will provide an early marker of the effectiveness and duration of protection of human papillomavirus vaccination at a population level.
Anogenital warts (AGWs) ARE caused by infection with the human papillomavirus (HPV). Approximately 90% result from infection with HPV types 6 and 11.1 Gardasil, the vaccine that has recently been licensed in many countries, provides protection against these types and 16 and 18, which are responsible for the majority of cervical cancers. To monitor the vaccine’s impact and assess its benefits, it is essential to have baseline population-based information on the epidemiology of AGWs. However, in most countries with a communicable disease reporting system, AGWs are not one of the regularly reported diseases. Current information on the incidence and prevalence of AGWs is based to a large extent on selected populations, such as those insured through private health plans, attending sexually transmitted disease clinics or university students.2,3 Furthermore, most studies have only included women. In Canada, there is only 1 published population-based study on the burden of AGWs,4 and the situation is just as bleak elsewhere.5 Despite the shortcomings in the reporting of AGWs, it is known that they are one of the most common sexually transmitted diseases in both developed and developing countries.6,7
This study used population-based medical claims and hospital separation records to estimate the AGWs incidence and prevalence rates in Manitoba during the period 1985 to 2004.
Data Sources and Definitions
We used nonidentifying information from databases (Manitoba Population Registry, medical claims, hospital discharges) maintained by Manitoba’s provincial health department. The Manitoba Population Registry includes all Manitobans who are eligible for provincial health insurance benefits. Since enrollment is free, virtually the entire population (>99%) is included. The medical claims record payment for services provided by physicians. Inpatient and day-patient hospital services provided to Manitobans in Manitoba and elsewhere are included in the hospitalization files. Outpatient and emergency department hospital services provided within Manitoba are not captured, although all out-of-province outpatient hospital services are included. However, outpatient services provided by fee-for-service physicians appear in the medical claims. Services provided by salaried or contract physicians are also in the medical claims, as they shadow bill Manitoba Health for administrative purposes.
People with AGWs were identified from the medical claims based on Manitoba tariff codes specific to condyloma (See Table, Supplemental Digital Content 1, which shows codes used for the identification of anogenital warts cases and their treatment, http://links.lww.com/A1011). These billing codes are analogous to the Current Procedure Terminology codes used in the United States. Identification of cases from the hospital records was more complicated, as coding practices changed over time (Table 1). We followed a method similar to that used by Insinga et al.6 Their Current Procedure Terminology codes (converted to International Classification of Diseases (ICD), Ninth Revision and 10th Revision [ICD-9, 10]) were used as a guideline, but we made some changes based on the availability of specific ICD codes (See Table, Supplemental Digital Content 2 and 3, which shows codes used for the identification of anogenital warts cases and their treatment, http://links.lww.com/A1012 and http://links.lww.com/A1013). For the ICD-10, we created a cross tabulation of all diagnosis by all procedure codes for the 9 months that these codes were used, and from this list identified those procedures related to AGW treatment.
Medical claims and hospitalization records were linked using a scrambled unique Personal Health Identification Number. The study was approved by the University of Manitoba’s Health Research Ethics Board and Manitoba Health’s Heath Information Privacy Committee.
Episodes of Care
In determining an episode of care, a wider selection of tariff codes was used than just those stating warts or condyloma. Any hospitalization or medical claim that had a specific wart tariff followed by another claim within 2 weeks that had a diagnosis of ICD-9 078 (other diseases due to viruses and Chlamydiae) and one of the tariffs listed in Table 4 (See Table, Supplemental Digital Content 4, which shows codes used for the identification of anogenital warts cases and their treatment, http://links.lww.com/A1014) were considered to be part of the treatment episode. If a similar combination of diagnosis and tariff codes occurred in the subsequent 2 weeks (i.e., weeks 3–4), then the episode length was extended. An episode was considered to be over once a 12-month period had elapsed without an AGW related claim or hospitalization.
Incidence and Prevalence
For incidence and prevalence, individuals could be counted more than once. An episode of care was considered to be incident if it was preceded by a 12-month interval free of AGWs care. The Manitoba Population Registry includes dates of death or emigration from the province. Therefore, it was possible to identify people who had been diagnosed with AGWs and who were alive and living in Manitoba at a particular point in time. A person was considered to be prevalent if they were experiencing an episode of AGWs on December 31.
The annual population figures used to derive the rates were taken from the Manitoba Population Registry. Incidence and prevalence rates were age-standardized to the 1991 Canadian population.
A total of 24,982 Manitobans were diagnosed with AGWs during the period 1985 to 2004 and they experienced 29,882 episodes. The majority of episodes (83.0%) were only identified from the medical claims. Hospital records alone accounted for 4.4% of the episodes, while 12.6% of episodes were identified in both the medical claims and hospitalization records.
For both men and women the annual age-standardized incidence rate peaked in 1992 (men, 149.9/100,000; women, 170.8/100,000) (Fig. 1). The male rate declined until 1999, but increased thereafter. The female rate also declined after 1991, but started to increase again in 2003 (2004—men, 154.0/100,000; women, 120.0/100,000).
Between 1985 and 2004 the incidence rate in almost all age groups increased for men, but decreased for women. Consequently, the male:female incidence rate ratio steadily increased from 0.75 in 1985 to 1.25 in 2004. Men have had a higher incidence rate than women since 2000.
The age at diagnosis ranged from 0 to 97 years. In all years, women aged 20 to 24 had the highest incidence rate. For men, this was also the case with the exception of the years 1997 to 1999 and 2001, when those aged 25 to 29 had the highest rate. For the period 2000 to 2004, at ages 20 to 24 the incidence rate was 391.9/100,000 for men and 466.3/100,000 for women (Fig. 2). With the exception of ages 10 to 24, men had a higher incidence rate than women at all ages.
On December 31, 2004, 1837.0/100,000 Manitobans (men, 1664.0/100,000; women, 2004.9/100,000) had been diagnosed with AGWs at sometime during the period 1984 to 2004 and 146.5/100,000 were experiencing a current episode (men, 165.2/100,000; women, 128.4/100,000).
The male and female prevalence rates peaked in 1992 (men, 180.2/100,000; women, 199.9/100,000) (Fig. 3). The rate decreased until the early 2000s, but has been increasing since then. The 2004 prevalence rate for men surpassed the peak reached in 1992. The male:female prevalence rate ratio increased from 0.76 in 1985 to 1.30 in 2004.
During the period 2000 to 2004 the prevalence rates of current AGWs peaked at ages 20 to 24 years in women (570.3/100,000) and ages 25 to 29 years in men (463.4/100,000) (Fig. 4). At ages 15 to 19 years the prevalence was 3.6 times higher in women than men. However, with the exception of ages 15 to 24, men had higher rates than women. Although the prevalence rates were low for the elderly, among those 60 years of age and over the rate was 2 or more times greater in men than women.
Over the 20-year period 1985 to 2004, 25,000 Manitobans were diagnosed with AGWs. Although AGWs generally do not warrant hospitalization, 17.0% of cases did have at least 1 hospitalization during their episode and 4.4% of cases were only identified from hospital discharge records. Another Canadian study found that 9% of cases had been hospitalized.4
There were similar trends in the incidence and prevalence rates. For both men and women, the rates increased from 1985 and reached a peak in 1992. The rates decreased until the late 1990s or early 2000s, but increased again in the last few years for which data were available. Prevalence was not much higher than incidence as the mean length of completed episodes was short (men, 69.8 days; women, 54.7 days).
Although comparison with other studies is difficult due to different case definitions, time periods, age groups included and sources of ascertainment, increases in incidence have been reported elsewhere in Canada4 and in other countries, including the United States,2,8,9 the United Kingdom,10 Australia,11 and Denmark.12 In England and Wales, there was a mostly continuous increase in the number and rate of cases for both men and women attending genitourinary medical clinics over the period 1971 to 2005.10,13 However, a study based on visits to sentinel general practices found little change in incidence between 1994 and 2001.14 The 1 study that we were able to identify that had examined prevalence trends also found an increase (1998–2006).4
The incidence rates found in a Canadian study for the period 1999 to 20064 and in 2 US studies based on the medical records of privately insured patients for 1999 and 2004 were comparable to Manitoba’s.15,16 A third US study found higher incidence rates in 1998 to 2001; however, it only included those aged 15 to 59 years.2 Estimates from the United Kingdom,17 France,18 Sweden,19 and Australia20 suggest the incidence rates are higher there than in Canada and the United States.
On December 31, 2004, 0.17% of men and 0.13% of women in Manitoba were experiencing a current diagnosed episode. A British Columbia study, also based on administrative data, found a similar prevalence (2006—men, 0.16%; women, 0.15%).4 Other Canadian studies in Ontario (1998–1999, 15 to 49 years of age)21 and Quebec (1975–1979, 11–71+ years of age)22 found prevalence to range between 1.1 and 1.7%; however, they were based on women having a Pap test, which would increase the likelihood of detection.
There are large variations in the reported prevalence of AGWs between countries, partly due to the different population subgroups studied and methods employed (e.g., self-report). The prevalence in 2000 among private health plan members in the United States was remarkably similar to Manitoba (0.17% for both men and women).6 Koutsky et al. estimated the overall prevalence in the United States in 1987 among men and women aged 15 to 49 years to be 1%.23 In Australia, in 2000–2001, 0.5% of men and 0.3% of women aged 16 to 59 self-reported having been diagnosed with genital warts in the last 12 months.24 The 12 month self-reported prevalence rate among Scandinavian women aged 18 to 45 years was substantially higher (1.3%).3
The male:female rate ratios for incidence and prevalence increased in Manitoba. The rates have been higher for men than women since 2000. Higher incidence rates for men than women have also been reported for British Columbia (1999–2006),4 the United States (1998–2001),2 and United Kingdom (1971–2005).13,17 Other incidence studies in the United States (1999, 2004)15,16 and Australia (2000–2006)20 found lower rates in men than women. Recent prevalence studies in the United States6 and Australia24 have found the rate to be slightly higher in men than women.
Among women, those aged 20 to 24 years had the highest incidence rates in all years. Men of this age also tended to have the highest rates, although in some years they were highest for those aged 25 to 29 years. Early studies found that the peak incidence rates in women preceded those in men by 5 to 6 years.25 Various Canadian and American studies also found the rates to be highest in the 20 to 29 year olds.2,4,8,9,15 In contrast, in England and Wales (1990–1994)13 and Sweden (1989–1990)19 the female rates have been reported to peak at 15/16 to 19 years of age.
For the period 2000 to 2004 prevalence was highest in men aged 25 to 29 years (0.46%) and in women 20 to 24 years of age (0.57%). Similar findings have been reported in the United States for 2000 (men: 25–29, 0.50%; women: 20–24, 0.62%).6 The prevalence among screened women aged 21 to 29 years in Washington State between 1984 and 1987 was 0.8%.26 Among sexually active Norwegian women aged 16 to 23 years prevalence was markedly higher (3.9%).27
Possible Reasons for Patterns
For men28,29 and women,3,30,31 one of the most consistently reported risk factors for AGWs has been sexual behaviour, particularly a greater number of sex partners. Smoking,3,11,28,31,32 oral contraceptive use,3,11,32 and marital status11,28–30 have also been found to be associated with increased risk, although less consistently. The changing AGW trends in Manitoba may have resulted from changes in these risk factors. To our knowledge, no Canadian study has examined trends in the risk factors for AGWs.
The rising sex ratio for AGWs is consistent with an increase in the sex ratio for chlamydia, gonorrhea, and syphilis in Canada between 1997 and 2004.33 It has been suggested that a changing sex ratio may be a surrogate marker of changes in sexual behaviors among men who have sex with men (MSM).34 The MSM population appears to be increasing in Canada, although this could be partly due to more open disclosure of sexual practices.35 Coupled with this are the reports of increased riskier sexual practices among these men.36,37 These factors may have contributed to the increasing incidence and prevalence of AGWs in men relative to women.
Age-specific variations in AGW rates between men and women may result more from health care behavior than biology,26 with women utilizing health services earlier and more frequently for such things as cervical screening, birth control prescriptions and pregnancy. Gender differences in HPV prevalence may also have contributed to the higher AGWs rates in older men than women. Two reviews of the global prevalence of HPV in women found it was highest in young women.38,39 This has been observed for both high and low oncogenic risk HPV.40,41 In contrast, in men, the overall and high-risk penile and scrotal HPV prevalence tends to be more consistent across age groups, whereas for low risk HPV prevalence appears to increase with age.42,43 The prevalence of anal HPV has been reported to be lower among younger heterosexual men than older ones.44 However, among MSM there was no age pattern, which may be attributed to their greater number of new sexual partners.45,46
Study Limitations and Strengths
This study has a number of limitations. Diagnosed cases were considered to be a proxy for incidence and prevalence. The true rates were underestimated to the extent that the AGWs were undetected or that people did not seek treatment for their AGWs. Such information is not available for Canada, but in the United States 10% declined treatment,8 whereas in Australia 7.4% of respondents stated they did not obtain treatment for their AGWs and a further 0.7% treated themselves.24 Given that virtually every resident in Manitoba is covered by the provincial health insurance plan, the cost of treatment will not be a barrier to seeking service. Embarrassment, inconvenience, and fear of treatment are possible reasons for not seeking treatment.6 Incomplete shadow billing by physicians who are not fee-for-service47 and the exclusion of emergency department visits from the hospital database would also lead to an underestimate of AGWs cases. However, most Manitoba physicians are fee-for-service and the number of people attending emergency for treatment of AGWs would be minimal.
Although not without problems, the overall quality of the Manitoba administrative databases has been found to be satisfactory.47 By using administrative data we were limited by the coding practices of physicians, hospitals and coders, and changes in these practices over time. The accuracy of the ICD codes and the completeness of the diagnoses captured in hospital discharge files have been questioned.48,49 Although cases identified through hospital records constituted a small proportion of all cases, a directive issued in 2001 to stop coding minor procedures such as excision of skin lesions, would have resulted in fewer cases being diagnosed in hospitals. Reliance on administrative data meant that cases were based on clinical findings rather than being confirmed by a laboratory. However, studies have found that there is good correlation between the diagnosis of genital warts based on a physical examination and histologic results.50
Our definitions relating to episodes would have affected the reported number of episodes. Currently there are no established time criteria to differentiate new or persistent infections.51 Without continued monitoring of an individual’s HPV status, it is impossible to determine if an episode is the result of a new or existing infection. We chose a 12-month treatment free period to define a new episode as studies have shown that most HPV 6 and 11 infections are cleared within 12 months, and thus, an episode after 12 months of no treatment may well be a new HPV infection.52,53 Other studies have also used 12 months in defining episodes.2,6 Selecting a longer period would lower the incidence and increase the prevalence.
A major strength of our study is that it included physician and hospital records and is the first to provide long-term population-based descriptive epidemiologic information on men and women diagnosed with AGWs. There have been very few population-based studies.3 Our study is free from the selection bias that studies based on selected population groups have, and should be more generally representative of populations with a similar medical system. Using medical records also eliminated the potential biases of self-report.54
The incidence and prevalence of AGWs has been increasing in recent years in Manitoba. AGWs have been shown to have a psychosocial impact on those infected and to lead to a reduced quality of life.55–57 As such, AGWs not only represent a substantial burden to the health care system, but also to those infected, and their prevention should be considered when setting goals of an HPV immunization program. Information on the changing incidence and prevalence of AGWs is important for the planning of policies and programs related to sexually transmitted infections and to the HPV vaccine. The results provide a baseline to assess the future impact of the vaccine on the burden of AGWs in Manitoba. Given the lengthy period of time between exposure to HPV and the development of cervical cancer, monitoring the future trends in AGWs will provide an early marker of the effectiveness and duration of protection of HPV vaccination at a population level and thus an indicator of the success of an HPV vaccination program. Among vaccinated women, it may be possible to observe a decrease in the incidence of AGWs in the first year after the start of sexual activity. However, observing a change at a population level will take longer, as it will depend on the uptake of the vaccine and on the sexual behavior of those vaccinated and their HPV status at the time of vaccination.
1. Greer CE, Wheeler CM, Ladner MB, et al. Human papillomavirus (HPV) type distribution and serological response to HPV type 6 virus-like particles in patients with genital warts. J Clin Microbiol 1995; 33:2058–2063.
2. Koshiol JE, Laurent SA, Pimenta JM. Rate and predictors of new genital warts claims and genital warts-related healthcare utilization among privately insured patients in the United States. Sex Transm Dis 2004; 31:748–752.
3. Kjaer SK, Tran TN, Sparen P, et al. The burden of genital warts: A study of nearly 70,000 women from the general female population in the 4 Nordic countries. J Infect Dis 2007; 196:1447–1454.
5. Cates W Jr. Estimates of the incidence and prevalence of sexually transmitted diseases in the United States. Am Social Health Association Panel. Sex Transm Dis 1999; 26(suppl):S2–S7.
6. Insinga RP, Dasbach EJ, Myers ER. The health and economic burden of genital warts in a set of private health plans in the United States. Clin Infect Dis 2003; 36:1397–1403.
7. Sonnex C, Lacey CJ. The treatment of human papillomavirus lesions of the lower genital tract. Best Pract Res Clin Obstet Gynaecol 2001; 15:801–816.
8. Chuang TY, Perry HO, Kurland LT, et al. Condyloma acuminatum in Rochester, Minnesota, 1950–1978. I. Epidemiology and clinical features Arch Dermatol 1984; 120:469–475.
9. Becker TM, Stone KM, Alexander ER. Genital human papillomavirus infection. A growing concern. Obstet Gynecol North Am 1987; 14:389–396.
11. Schofield MJ, Minichiello V, Mishra GD, et al. Sexually transmitted infections and use of sexual health services among young Australian women: Women’s Health Australia study. Int J STD AIDS 2000; 11:313–323.
12. Kjaer SK, Lynge E. Incidence, prevalence and time trends of genital HPV infection determined by clinical examination and cytology. IARC Sci Publ 1989; 94:113–124.
13. Simms I, Fairley CK. Epidemiology of genital warts in England and Wales: 1971 to 1994. Genitourin Med 1997; 73:365–367.
14. Simms I, Fleming DM, Lowndes CM, et al. Surveillance of sexually transmitted diseases in general practice: A description of trends in the Royal College of General Practitioners Weekly Returns Service between 1994 and 2001. Int J STD AIDS 2006; 17:693–698.
15. Insinga RP, Dasbach EJ. The clinical incidence of Condyloma acuminata in a set of private US health plans. In: Program and Abstracts of the Clinical Workshop and 20th International Papillomavirus Conference. 231, 2002; Paris, France.
16. Singhal PK, Schabert V, Insinga RP, et al. The incidence and healthcare cost of genital warts in a commercially insured population in the United States. In: Abstract Book of the 24th International Papillomavirus Conference and Clinical Workshop. 200, 2007; Beijing, China.
17. Cassell JA, Mercer CH, Sutcliffe L, et al. Trends in sexually transmitted infections in general practice 1990 to 2000: Population based study using data from the UK general practice research database. BMJ 2006; 332:332–334.
18. Monsonego J, Breugelmans JG, Bouee S, et al. [Anogenital warts incidence, medical management and costs in women consulting gynaecologists in France.] Gynecol Obstet Fertil 2007; 35:107–113.
19. Persson G, Andersson K, Krantz I. Symptomatic genital papillomavirus infection in a community. Incidence and clinical picture. Acta Obstet Gynecol Scand 1996; 75:287–290.
20. Conway EL, Stein AN, Britt H, et al. Genital warts and associated health care in general practice in Australia. In: Abstract Book of the 24th International Papillomavirus Conference and Clinical Workshop. 198, 2007; Beijing, China.
21. Sellors JW, Mahony JB, Kaczorowski J, et al. Prevalence and predictors of human papillomavirus infection in women in Ontario, Canada. Survey of HPV in Ontario Women (SHOW) Group. CMAJ 2000; 163:503–508.
22. Meisels A, Morin C. Human papillomavirus and cancer of the uterine cervix. Gynecol Oncol 1981; 12(pt 2):S111–S123.
23. Koutsky L. Epidemiology of genital human papillomavirus infection. Am J Med 1997; 102:3–8.
24. Grulich AE, de Visser RO, Smith AM, et al. Sex in Australia: Sexually transmissible infection and blood-borne virus history in a representative sample of adults. Aust N Z J Public Health 2003; 27:234–241.
25. zur Hausen H. Human papillomaviruses and their possible role in squamous cell carcinomas. Curr Top Microbiol Immunol 1977; 78:1–30.
26. Koutsky LA, Galloway DA, Holmes KK. Epidemiology of genital human papillomavirus infection. Epidemiol Rev 1988; 10:122–163.
27. Turpin J, Liaw KL, Overness T, et al. The incidence and prevalence of genital warts and HPV infection in young sexually active Norwegian women. In: Program and Abstracts of the Clinical Workshop and 20th International Papillomavirus Conference. 282, 2002; Paris, France.
28. Wen LM, Estcourt CS, Simpson JM, et al. Risk factors for the acquisition of genital warts: are condoms protective? Sex Transm Infect 1999; 75:312–316.
29. Van Den Eeden SK, Habel LA, Sherman KJ, et al. Risk factors for incident and recurrent condylomata acuminata among men. A population-based study. Sex Transm Dis 1998; 25:278–284.
30. Habel LA, Van Den Eeden SK, Sherman KJ, et al. Risk factors for incident and recurrent condylomata acuminata among women. A population-based study. Sex Transm Dis 1998; 25:285–292.
31. Munk C, Svare EI, Poll P, et al. History of genital warts in 10,838 women 20 to 29 years of age from the general population. Risk factors and association with Papanicolaou smear history. Sex Transm Dis 1997; 24:567–572.
32. Daling JR, Sherman KJ, Weiss NS. Risk factors for condyloma acuminatum in women. Sex Transm Dis 1986; 13:16–18.
33. Public Health Agency of Canada. 2004 Canadian sexually transmitted infections surveillance report. Can Commun Dis Rep 2007; 33(suppl 1):1–69.
34. Beltrami JF, Shouse RL, Blake PA. Trends in infectious diseases and the male to female ratio: possible clues to changes in behavior among men who have sex with men. AIDS Educ Prev 2005; 17(suppl B):49–59.
35. Tjepkema M. Health care use among gay, lesbian and bisexual Canadians. Health Rep 2008; 19:53–64.
36. Lampinen TM, Chan K, Craib KJP, et al. Trends in condom use and HIV-1 seroincidence in a cohort of young men who have sex with men (MSM) in Vancouver, 1997–2002. Can J Infect Dis Med Microbiol 2003; 14(suppl SA):41A.
37. George C, Alary M, Otis J, et al. Nonnegligible increasing temporal trends in unprotected anal intercourse among men who have sexual relations with other men in Montreal. J Acquir Immun Defic Syndr 2006; 41:365–370.
38. de Sanjosé S, Diaz M, Castellsague X, et al. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: A meta-analysis. Lancet Infect Dis 2007; 7:453–459.
39. Smith JS, Melendy A, Rana RK, et al. Age-specific prevalence of infection with human papillomavirus in females: A global review. J Adolesc Health 2008; 43(suppl 1):S5–S25, S25 e1–e41.
40. Dunne EF, Unger ER, Sternberg M, et al. Prevalence of HPV infection among females in the United States. JAMA 2007; 297:813–819.
41. Kjaer SK, Breugelmans G, Munk C, et al. Population-based prevalence, type- and age-specific distribution of HPV in women before introduction of an HPV-vaccination program in Denmark. Int J Cancer 2008; 123:1864–1870.
42. Giuliano AR, Lazcano-Ponce E, Villa LL, et al. The human papillomavirus infection in men study: Human papillomavirus prevalence and type distribution among men residing in Brazil, Mexico, and the United States Cancer Epidemiol Biomarkers Prev 2008; 17:2036–2043.
43. Giuliano AR, Lu B, Nielson CM, et al. Age-specific prevalence, incidence, and duration of human papillomavirus infections in a cohort of 290 US men. J Infect Dis 2008; 198:827–835.
44. Nyitray A, Nielson CM, Harris RB, et al. Prevalence of and risk factors for anal human papillomavirus infection in heterosexual men. J Infect Dis 2008; 197:1676–1684.
45. Chin-Hong PV, Vittinghoff E, Cranston RD, et al. Age-related prevalence of anal cancer precursors in homosexual men: The EXPLORE study. J Natl Cancer Inst 2005; 97:896–905.
46. Chin-Hong PV, Vittinghoff E, Cranston RD, et al. Age-specific prevalence of anal human papillomavirus infection in HIV-negative sexually active men who have sex with men: The EXPLORE study. J Infect Dis 2004; 190:2070–2076.
47. Roos LL, Gupta S, Soodeen RA, et al. Data quality in an information-rich environment: Canada as an example. Can J Aging 2005; 24(suppl 1):153–170.
48. O’Malley KJ, Cook KF, Price MD, et al. Measuring diagnoses: ICD code accuracy. Health Serv Res 2005; 40(pt 2):1620–1639.
49. Surján G. Questions on validity of International Classification of Diseases-coded diagnoses. Int J Med Inform 1999; 54:77–95.
50. Beutner KR, Reitano MV, Richwald GA, et al. External genital warts: report of the Am Medical Association Consensus Conference. AMA Expert Panel on External Genital Warts. Clin Infect Dis 1998; 27:796–806.
51. Trottier H, Franco EL. The epidemiology of genital human papillomavirus infection. Vaccine 2006; 24(suppl 1):S1–S15.
52. 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.
53. 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.
54. Wiley DJ, Grosser S, Qi K, et al. Validity of self-reporting of episodes of external genital warts. Clin Infect Dis 2002; 35:39–45.
55. Garland S, Ung L, Conway EL, et al. The Australian Women’s Health Survey: assessing the psychosocial burden of HPV related illness and preventative interventions. In: Abstract Book of the 24th International Papillomavirus Conference and Clinical Workshop. 199, 2007; Beijing, China.
56. Woodhall S, Ramsey T, Cai C, et al. Estimation of the impact of genital warts on health-related quality of life. Sex Transm Infect 2008; 84:161–166.
57. Senecal M, Maunsell E, Brisson M, et al. Quality of life lost associated with external genital warts: Preliminary baseline analyses from a prospective cohort study. In: Abstract Book of the 24th International Papillomavirus Conference and Clinical Workshop. 194, 2007; Beijing, China.
Supplemental Digital Content
© Copyright 2009 American Sexually Transmitted Diseases Association
What does "Remember me" mean?
By checking this box, you'll stay logged in until you logout. You'll get easier access to your articles, collections,
media, and all your other content, even if you close your browser or shut down your
To protect your most sensitive data and activities (like changing your password),
we'll ask you to re-enter your password when you access these services.
What if I'm on a computer that I share with others?
If you're using a public computer or you share this computer with others, we recommend
that you uncheck the "Remember me" box.
Data is temporarily unavailable. Please try again soon.