Knowledge about infection with human papillomavirus: A systematic review

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Preventive Medicine 46 (2008) 87 – 98 www.elsevier.com/locate/ypmed

Knowledge about infection with human papillomavirus: A systematic review Stefanie J. Klug ⁎, Meike Hukelmann, Maria Blettner Institute of Medical Biostatistics, Epidemiology and Informatics, Hospital of the University of Mainz, 55101 Mainz, Germany Available online 14 September 2007

Abstract Objective. Human papillomavirus (HPV) is a necessary cause of cervical cancer and genital warts. The aim of this systematic literature review was to provide an overview of knowledge about HPV infection among the public, students, patients and health professionals. Method. PubMed searches were performed and the results of studies were reported by age, gender, study population, country, recruitment score and year of study conduct. The recruitment score covered the mode of recruitment, study size and response rate. Results. We included 39 studies published between 1992 and 2006 covering a total of 19,986 participants. The proportion of participants who had heard of HPV varied from 13% to 93%. Understanding that HPV is a risk factor for cervical cancer depended on whether the question was closed (8–68%) or open (0.6–11%). Between 5% and 83% knew about the association of HPV and (genital) warts. HPV was often mistaken with other sexually transmitted viruses. Health professionals and women had better knowledge about HPV than other participants. Conclusion. Overall, the knowledge of the general public about HPV infection is poor. Efforts should be increased to give sufficient and unbiased information on HPV infection to the general public. © 2007 Elsevier Inc. All rights reserved. Keywords: Health knowledge; Attitudes; Practice; Papillomavirus; Human; Cervical cancer; Genital warts; Vaccines; Review

Introduction Infection with human papillomavirus (HPV) is one of the most common sexually transmitted infections (Braly, 1996). More than 100 different HPV types have been described, about 30 of which infect the genital system (de Villiers et al., 2004). High-risk types of HPV are a necessary cause of cervical cancer (zur Hausen, 1991; Munoz et al., 1992; Schiffman et al., 1993; Walboomers et al., 1999; Munoz et al., 2003; Cogliano et al., 2005), which is the second commonest cancer in women worldwide (Ferlay et al., 2004). Additionally, some low-risk HPV types cause considerable morbidity by causing benign genital warts (Trottier and Franco, 2006). In the USA in 2000, only 2% of persons aged 18 and older named “HPV” or “human papillomavirus” when asked what sexually transmitted diseases they knew, and only 28% had heard of HPV (The Kaiser Family Foundation, 2000). We performed a population-based survey in Bielefeld, Germany, in 2000 and found that knowledge about the risk factors for cervical cancer was poor. Only 3.2% of the participants (women aged 25–75) named ⁎ Corresponding author. Fax: +49 6131 172968. E-mail address: [email protected] (S.J. Klug). 0091-7435/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ypmed.2007.09.003

“HPV”, “papillomavirus” or “virus” as a risk factor, and only 1.5% had heard of “HPV” or “papillomavirus” (Klug et al., 2005). A quadrivalent vaccine against HPV 6, 11, 16 and 18 has been approved in 2006 by the US Food and Drug Administration, the European Medicines Agency and other official agencies around the world. Avaccine that protects against HPV 16 and 18 is expected to be licensed in the near future (Arbyn and Dillner, 2007). Both prophylactic vaccines against HPV have been assessed in large clinical trials and have been shown to be well tolerated and efficacious (Koutsky et al., 2002; Harper et al., 2004; Villa, 2005; Arbyn and Dillner, 2007; Kaufmann and Schneider, 2007). There is evidence that acceptance of HPV vaccination is increased when parents or young women were well informed about the risks and benefits (Kahn et al., 2003; Davis et al., 2004), although this was not found consistently (Dempsey et al., 2006). If women are tested for HPV infection in the frame of cervical cancer screening, it is important that they receive adequate information on HPV and that they understand the implications of an HPV infection (Cuzick et al., 2006). We performed a systematic review of various literature databases to determine knowledge about HPV infections and HPV as a risk factor for cervical cancer. The results of all the studies included are presented by age and gender, by study

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population, by country, by recruitment score and by year of study conduct in order to determine further needs for education on and prevention of HPV infection.

ages (15 years and above). In addition, studies were categorized according to the selection of participants: the general public, students, patients and health professionals, the latter including physicians, nurses, nurse practitioners and teachers of health courses. An attempt was made to analyze physicians separately.

Methods

Response rate

Search strategy

Information on participation was abstracted from each publication. For comparison, the response rate in each study was recalculated, when possible, with the formula of Slattery et al. (1995). In some publications, however, the numbers for non-participation (refusal, not eligible, not contacted) were not listed separately or remained unclear. If the data necessary for recalculation were not available, the participation rates given in the publication were extracted. If no proportion for participation was given or could be recalculated, the response rate was classified as missing.

Literature searches in PubMed (last updated April 2007) were conducted with 11 combinations of keywords: “HPV attitudes”, “HPV attitude”, “HPV knowledge”, “HPV health knowledge”, “HPV education”, “HPV practice”, “HPV health practice”, “HPV health education”, “HPVawareness”, “HPVethnic groups” and “HPV health behavior”. Replacing the term “HPV” by “papillomavirus” yielded additional publications. In total, 108 publications were identified from PubMed, and six further publications were found in the reference lists of these publications. The psychological database PsyDok was searched with the keywords “HPV” and “papillomavirus”, but no publications were found.

Inclusion criteria All studies of knowledge about the existence of HPV, about HPV as a risk factor for cervical cancer, about the symptoms of an HPV infection and about transmission of HPV were included if published before January 2007. No limitations were applied on study size, study population or country in which they were conducted.

Recruitment score We attempted to assess the quality of recruitment of the study sample and also used this information as a surrogate for potential selection bias on the basis of strict epidemiological criteria. Scores were calculated for three categories: recruitment of participants, response rate and number of study subjects (Fig. 1). The scores from the three categories were added, yielding scores classified as: low, zero to four points; medium, five to eight points; and high, nine to twelve points. No recruitment score was assigned to studies based on health professionals or focus groups.

Statistical methods Exclusion criteria We excluded case reports, general reviews, letters to the editor, editorials and articles in languages other than English. Studies in which participants were given basic information before they answered the questionnaire and studies that resulted in general knowledge scores were also excluded.

Linear regression was performed to examine the association between year of study conduct and knowledge of HPV infection. Spearman's correlation coefficient and the corresponding p value were calculated. All p values were two-sided and considered statistically significant if below 0.05. This was an exploratory analysis.

Categorization of studies

Results

The studies were divided into four groups according to the age and gender of the study subjects. Group 1 comprised all studies of women up to the age of 30 years, also including studies of female students with no indication of age and some female students over 30. Group 2 comprised studies of women of all ages (13 years and above). Group 3 comprised studies of young men and women up to the age of 30 years, also including studies of students with no indication of age and some students over 30. Group 4 comprised studies of men and women of all

Overall, 114 articles dealing with knowledge about HPV were identified, of which 75 were excluded for the following reasons: knowledge questions not fitting our inclusion criteria (eight); focus groups without quantitative data (13); general reviews, reports of another publication, letters to the editor or editorials without original data (23); case report (one); language

Fig. 1. The recruitment score consists of three items: mode of recruitment, response rate and study size.

Table 1 Characteristics of 39 studies on knowledge about HPV infection published between 1992 and 2006 involving 19,986 total participants Reference

Study region, country

Year(s) of study Age (years) conduct

Gender

Ethnicity

Survey instrument

Number of participants

Study population

Recruitment

Response rate

Vail-Smith and White (1992) Linnehan et al. (1996)

Southeast, USA

1989

Mostly 18–23

Female

100%

≥ 25

Female and male

All eligible college-based health centers

53%

Martinez et al. (1997)

Orange County, USA

1991–1992

42 (mean)

30

1995

≥ 25

Questionnaire assumed to be sent by mail

444

Ramirez et al. (1997)

Not specified, USA

1992

18–22

Female

Eastern Cape, South Africa

1997 a

15–40

Female

Questionnaire filled in at appointment or dormitory floor meeting Questionnaire distributed in residences

110

Buga (1998)

54% Caucasian, 16% Asian, 13% Hispanic Not specified

260

University students

Hasenyager (1999)

Not specified, USA

1996–1997

18–57

Female

Not specified

Questionnaire filled in at doctor's visit

154

Yacobi et al. (1999)

Florida, USA

1996

25 (median)

81% Caucasian

Questionnaire sent by mail

289

Baer et al. (2000)

New England, USA

1996 a

≥ 18

76% Caucasian, 16% Asian

Questionnaire sent by mail

322

Dell et al. (2000)

Toronto, Canada

1999 a

≥ 15

Mixed

Hoover et al. (2000) Mays et al. (2000)

New Jersey, USA Chicago and Indianapolis, USA

1998 1998 a

Questionnaire filled in during class Face-to-face interview Face-to-face interview

Lambert (2001)

New York, USA

Not available

15–28 14–18 (Indianapolis) 20–50 (Chicago) ≥ 18

Female and male Female and male Female and male Female Female

Patients at university health center; students, eligible if presenting for yearly gynecological examinations University students

Apparently convenience sample Random sample from Australian Medical Publishing Company national database All eligible students, additional convenience sample Convenience sample (every second, but next one if person refused) Not clearly stated

Not available

Victoria, Australia

60% Caucasian, 20% Asian, 10% Latino Not specified

Face-to-face interview

Mulvey et al. (1997)

Female and male Female and male

University students enrolled in health courses Physicians or nurse practitioners able to diagnose and treat HPV, working at college-based health center with an undergraduate population of at least 3400; physician assistants excluded Physicians based at University of California, Irvine, and community of Irvine Registered general practitioners, excluded if over the retirement age of 65 or with fewer than 1500 consultations per year University students

Random sample

1994 a

Questionnaire answered on computer sheet Questionnaire by mail

263

Not specified, USA

90% Caucasian, 8% African American Not specified

Not specified

Lazcano-Ponce et al. (2001) Wardle et al. (2001)

Cuernavaca, Mexico

1998

15–49

Female and male Female

3.2% or 35% b,c

99%

First-year university students

523

Senior high school students

Convenience sample

Not available

60 20 Indianapolis, 20 Chicago

Young women at the beach Patients in waiting rooms at health clinics, low socioeconomic status

Convenience sample Convenience sample

Not available Not available

60

Students at private college

Convenience sample

100% e

Not specified

Questionnaire filled in during class Face-to-face interview

880

Population-based sample of households

Population-based random sample

86%

Not specified

Interview

3693

Population-based sample

Population-based random sample

Not available

95% Caucasian Not specified

Questionnaire sent by mail Questionnaire sent by mail

400 108

All eligible employees Not stated

41% Not available

Mainly Caucasian

Questionnaire sent by mail Questionnaire sent by mail Questionnaire filled in at doctor's visit

163

University employees Teachers and nurses from high school and middle school Population-based sample

54%

222

University students

Population-based random sample Random sample

1032

Women attending a clinic

About 80% d

Questionnaire filled in at focus group

48

Low-income and minority women

Women during a certain time period in selected clinic sessions, unclear if consecutive Focus group

Questionnaire filled in during routine gynecological check-up, before lecture on risk factors for cervical cancer or during class

162

Women presenting to general practitioners for a routine gynecological check-up; women attending lecture on risk factors for cervical cancer, class of students in third year of biomedical science

Convenience sample

Not available

97% Caucasian 75% Caucasian (Indianapolis); 95% African American (Chicago)

1999 2000 2000

a

Gudmundsdottir et al. (2003) Philips et al. (2003)

Reykjavik, Iceland

2001

18–23

Female and male Female Female and male Female

Nottingham, England

Not available

18–23

Female

94% Caucasian

Waller et al. (2003)

London, England

2000–2002

≥ 16

Female

84% Caucasian

Anhang et al. (2004)

Not specified, USA

2002

18–81

Female

Baay et al. (2004)

Antwerp, Belgium

2003

39.6 (mean)

Female

40% Caucasian, 44% Hispanic, 13% African American Not available

22% b

S.J. Klug et al. / Preventive Medicine 46 (2008) 87–98

74% d

58% b

Not specified, United Kingdom Pitts and Clarke (2002) Northwest England Beatty et al. (2003) Vermont, USA

19–64 Not available

79% b,c

Random sample provided by registrar's office All eligible students

a

16 and above

143

44% b

Not applicable

89

(continued on next page)

90

Table 1 (continued) Reference

Study region, country

Year(s) of study conduct

Age (years)

Gender

Ethnicity

Survey instrument

Number of participants

Study population

Recruitment

Response rate

Boardman et al. (2004)

Providence, USA

2001

13–63

Female

Face-to-face interview

250

Patients at colposcopy clinic, cancer patients excluded

Consecutive patients

Not available

Holcomb et al. (2004) Lai et al. (2004)

Not specified, USA

2001

≥18 Not available

Patients at local university health service and family practice clinics Vietnamese physicians in northern California invited to education seminar

Convenience sample of consecutive patients Not clearly stated

About 80% d

2001

Questionnaire filled in at doctor's visit Questionnaire filled in at education seminar

289

Northern California, USA

Female and male Female and male

44% Caucasian, 28% Hispanic, 17% African American 71% Caucasian, 12% African American 100% Asian

Le et al. (2004)

Ottawa, Canada

2003 a

18–75

Female

Not specified

Face-to-face interview

100

Consecutive patients

Waller et al. (2004)

2002

≥16

Face-to-face interview

1937

1999

15–85

Female and male Female

93% Caucasian

Ackermann et al. (2005)

Not specified, United Kingdom Düsseldorf area, Germany

Mainly Caucasian

Questionnaire filled in at doctor's visit

2108

Chingang et al. (2005)

Port-of-Spain, Trinidad and Tobago

2003 a

Not available

Female and male

Not specified

Face-to-face interview

63

Klug et al. (2005) Philips et al. (2005)

Bielefeld, Germany East-central England

2000 Not available

25–75 20–64

Female Female

Mainly Caucasian 98% Caucasian

Questionnaire sent by mail Questionnaire distributed at doctor's visit or sent by mail

532 1244

Pruitt et al. (2005)

Texas, USA

2002–2003 a

18–79

Female

Face-to-face interview

175

Sharpe et al. (2005)

Southern Carolina, USA

2002–2003

19–63

Female

46% 34% 17% 32% 68%

Women with Pap smear result of ASCUS or LSIL seen at clinic Population-based sample of households Patients at routine visit at gynecologist, patients with known gynecological or breast malignancy excluded General practitioners and gynecologists in inner Port of Spain offering Pap smears Population-based sample Women eligible for cervical screening during routine (non-screening) consultations and women called for screening by Nottingham screening service Patients and community volunteers with abnormal Pap smear

Face-to-face interview

44

Baay et al. (2006)

Antwerp, Belgium

2004 a

Not available

Female and male

Not available

Questionnaire distributed during post-academic training session and during education at university

88

Daley et al. (2006)

Not specified, USA

2005

48 (mean)

Not available

Victoria, Australia

2004 a

18–30

Not specified, USA

2004

47 (mean)

Male Not available and female

Questionnaire sent by mail or Internet Questionnaire distributed at doctor's visit Questionnaire sent by mail

294

Giles and Garland (2006) Irwin et al. (2006)

Female and male Female

Massad et al. (2006)

Illinois, USA

2003–2004 a

19–65

Female

71% Caucasian, 4% Hispanic, 25% African American

Questionnaire distributed at doctor's visit

178

Moreira et al. (2006)

Salvador City, Brazil

2002

16–23

Female

2% white, 26% black, 73% mixed

Face-to-face interview

204

Not available

All information was taken from original publications, except response rate which was recalculated wherever possible. a

Information obtained from authors.

b

Number of subjects excluded because of incomplete questionnaire unknown.

c

Number of ineligible subjects unknown.

d

From publication.

e

100% response rate was achieved because questionnaires were distributed in a classroom and filled in directly.

f

Number of subjects who could not be contacted unknown.

60 2980

Patients at primary health clinics, diagnosed high-risk HPV positivity, abnormal Pap smear General practitioners during post-academic training session not concerning cervical cancer, general practitioners still in training coming back to university for further education US pediatrician network, excluded if spending b 50% of their time in primary care Women attending a local university health service or cervical dysplasia clinic US clinician database (physicians, nurse midwives, nurse practitioners, physician assistants) in specialties that often offer Pap screening (gynecology and obstetrics; family, general, internal or adolescent medicine) Women attending colposcopy clinics for evaluation of abnormal cytology; low socioeconomic status Women in waiting room of gynecological clinic; low socioeconomic status

Population-based random sample Women visiting 23 office-based gynecologists

Not available (only those attending education seminar) 75% d 71% 73% c

All eligible

100% (of those who could be reached) f

Population-based random sample Women visiting 20 general practitioners and random sample of women called for screening

36% 28% b,c

Convenience sample

Not available

Convenience sample

Not available

Convenience sample

100% e

All eligible

68% b

Convenience sample

Not available

Random sample

70%

Consecutive patients

Not available

Consecutive sample

86%

S.J. Klug et al. / Preventive Medicine 46 (2008) 87–98

Caucasian, Hispanic, African American Caucasian, African American

34

S.J. Klug et al. / Preventive Medicine 46 (2008) 87–98

91

other than English (four); basic information about HPV given to participants before or during filling in the questionnaire (seven); data presentation inadequate for our review (eight); no examination of knowledge items (nine); and second publication on the same study (two). A total of 39 articles published between 1992 and 2006 met the inclusion criteria, did not fulfill any of the exclusion criteria and were therefore included in this systematic review (Table 1). In total, 19,986 participants were surveyed. The size of the studies differed substantially, and different modes of recruitment were used. The response rate varied from 3% to 100%. Most of the studies were conducted in the USA (20) and the United Kingdom (6).

participants had heard of HPV, of women of all ages (group 2), 15–31% had heard of HPV. Between 10 and 85% of the study participants knew that infection with HPV can be asymptomatic. More than two thirds of young women (group 1) knew that HPV is a sexually transmitted infection. Three studies were identified in which the results presented were restricted to participants who had heard of HPV (Baer et al., 2000; Waller et al., 2003; Holcomb et al., 2004) (data not shown). In these studies, 40% of women of all ages (group 2) confirmed the statement that HPV is the main cause of cervical cancer (Waller et al., 2003), and 18–72% knew that HPV is sexually transmitted.

Knowledge about HPV infection

Knowledge about HPV and cervical cancer

Knowledge about HPV infection varied widely within the groups and according to the questions asked (Table 2). In studies including young women (group 1), 13–93% of study

The association between HPV and cervical cancer was known by 8% to 68% of study participants of different age and gender (group 1 to group 4) if different possible answers were

Table 2 Knowledge about HPV infection by age and gender (health professionals excluded), reported in 25 studies Question

Heard of HPV…

HPV as a risk factor for cervical cancer was known by… (closed question)

Young women (group 1)

Women of all ages (group 2)

Young men and women (group 3)

Men and women of all ages (group 4)

% (reference)

% (reference)

% (reference)

% (reference)

13 (Vail-Smith and White, 1992) 20 (Mays et al., 2000) 23 (Hoover et al., 2000) 25 (Waller et al., 2003) 31 (Philips et al., 2003) 73 (Giles and Garland, 2006) a 93 (Giles and Garland, 2006) b 8 (Vail-Smith and White, 1992) c 10 (Moreira et al., 2006) c 16 (Baer et al., 2000) 33 (Giles and Garland, 2006) a 34 (Gudmundsdottir et al., 2003) 44 (Ramirez et al., 1997) 49 (Hasenyager, 1999) 51 (Philips et al., 2003) 55 (Boardman et al., 2004) 57 (Giles and Garland, 2006) b 68 (Buga, 1998)

15 (Mays et al., 2000) 27 (Anhang et al., 2004) 30 (Pitts and Clarke, 2002) 31 (Waller et al., 2003)

13 (Dell et al., 2000) 38 (Yacobi et al., 1999)

47 (Pruitt et al., 2005) 51 (Philips et al., 2005) 57 (Boardman et al., 2004)

13 (Baer et al., 2000) 27 (Yacobi et al., 1999) 53 (Lambert, 2001)

HPV as risk factor for cervical cancer was named by… (open question)

Participants who knew that HPV can be asymptomatic

Participants who knew that HPV is sexually transmitted

a

10 (Vail-Smith and White, 1992) 27 (Ramirez et al., 1997) 63 (Giles and Garland, 2006) a 73 (Giles and Garland, 2006) b 47 (Boardman et al., 2004) 63 (Gudmundsdottir et al., 2003) 67 (Moreira et al., 2006) 83 (Giles and Garland, 2006) b 84 (Ramirez et al., 1997) 87 (Giles and Garland, 2006) a

0.9 (Waller et al., 2004) 1.5 (Klug et al., 2005) d 1.9 (Lazcano-Ponce et al., 2001) 3.1 (Baay et al., 2004) 11 (Pitts and Clarke, 2002) 17 (Pitts and Clarke, 2002) 66 (Pruitt et al., 2005)

39 (Holcomb et al., 2004)

0.6 (Waller et al., 2004)

10 (Yacobi et al., 1999) 85 (Lambert, 2001)

30 (Pitts and Clarke, 2002) 47 (Boardman et al., 2004) 70 (Pruitt et al., 2005)

Women attending local university health service. Women attending cervical dysplasia clinic. c Closed question assumed, but not clearly stated. d In the publication, 3.2% was given which also included the word “virus”. Here, only “HPV” and “papillomavirus” were considered for comparability with the other studies. b

92

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pregiven and there was multiple choice (closed questions) (Table 2). When this knowledge was assessed using an open question, it was consistently lower (0.6–11%). Le and colleagues (2004) reported that 75% of women with an abnormal Pap smear had no or minimal knowledge of the role of HPV in the development of cervical cancer (data not shown). When study results were grouped by study population, a wide range of knowledge was found within the groups of students and patients (Table 3). Of the four studies with a population base, three used an open question to assess knowledge on HPV as a risk factor for cervical cancer (Lazcano-Ponce et al., 2001; Waller et al., 2004; Klug et al., 2005), and knowledge in the population was low (0.6–1.9%). Gudmundsdottir and colleagues used a closed question and 34% of the study population knew that HPV is a risk factor for cervical cancer (Gudmundsdottir et al., 2003). Nine studies addressed the knowledge of physicians, nurses and teachers of health courses about HPV infections (Table 1). Health professionals had considerably more knowledge than the other groups (Table 3). Between 82–100% and 59–87% of physicians knew that HPV is a risk factor for cervical cancer when a closed and open question was used, respectively (Linnehan

et al., 1996; Martinez et al., 1997; Lai et al., 2004; Chingang et al., 2005; Irwin et al., 2006; Baay et al., 2006). The 100% knowledge was obtained in a group of motivated physicians right before attending a seminar on cervical cancer topics (Lai et al., 2004). Additionally, 96% of experienced general practitioners with more than 1500 consultations per year knew that HPV is the sexually transmitted infection most commonly associated with cervical cancer (Mulvey et al., 1997). Half of these general practitioners saw patients with an STD at least once a month. In a study of US pediatricians, 68% knew that almost all cervical cancers are caused by HPV infection, while only 20% knew that genital warts are not caused by the same HPV types that cause cervical cancer (Daley et al., 2006). Teachers and nurses in middle and high schools in the USA had less knowledge than physicians. Only half approved the sentence that HPV was found in the cervices of most women with cervical cancer, and only 33% denied that most women with HPV will develop cervical cancer (Beatty et al., 2003). Knowledge about HPV by country Most studies have been performed in the USA and there was a wide range of knowledge (Table 4). No differences between

Table 3 Knowledge about HPV infection by participant group, reported for 28 studies Question

Heard of HPV…

Students

Patients

Physicians

Population-based

% (reference)

% (reference)

% (reference)

% (reference)

13 (Vail-Smith and White, 1992) 13 (Dell et al., 2000) 31 (Philips et al., 2003) 38 (Yacobi et al., 1999) 73 (Giles and Garland, 2006) a HPV as a risk factor for cervical 8 (Vail-Smith and White, 1992) b cancer was known by… 13 (Baer et al., 2000) (closed question) 27 (Yacobi et al., 1999) 33 (Giles and Garland, 2006) a 44 (Ramirez et al., 1997) 49 (Hasenyager, 1999) 51 (Philips et al., 2003) 53 (Lambert, 2001) 68 (Buga, 1998) HPV as a risk factor for cervical cancer was named by… (open question) Participants who knew that HPV 10 (Vail-Smith and White, 1992) can be asymptomatic 10 (Yacobi et al., 1999) 27 (Ramirez et al., 1997) 63 (Giles and Garland, 2006) a 85 (Lambert, 2001) Participants who knew that HPV 84 (Ramirez et al., 1997) is sexually transmitted 87 (Giles and Garland, 2006) a

a

18 (Mays et al., 2000) 31 (Waller et al., 2003) 93 (Giles and Garland, 2006)

10 (Moreira et al., 2006) b 39 (Holcomb et al., 2004) 47 (Pruitt et al., 2005) 51 (Philips et al., 2005) 57 (Boardman et al., 2004) 57 (Giles and Garland, 2006)

82 (Chingang et al., 2005) b, c 34 (Gudmundsdottir et al., 2003) 92 (Chingang et al., 2005) b, d 97 (Linnehan et al., 1996) e 98 (Irwin et al., 2006) 100 (Lai et al., 2004)

59 (Baay et al., 2006) 87 (Martinez et al., 1997)

0.6 (Waller et al., 2004) 1.5 (Klug et al., 2005) f 1.9 (Lazcano-Ponce et al., 2001)

66 (Pruitt et al., 2005) 83 (Daley et al., 2006) 73 (Giles and Garland, 2006) 97 (Irwin et al., 2006)

47 (Boardman et al., 2004) 67 (Moreira et al., 2006) 70 (Pruitt et al., 2005) 83 (Giles and Garland, 2006)

63 (Gudmundsdottir et al., 2003)

Women attending local University Health service. Closed question assumed, but not clearly stated. c General practitioners. d Gynecologists. e Including nurse practitioners. f In the publication, 3.2% was given which also included the word “virus”. Here, only “HPV” and “papillomavirus” were considered for comparability with the other studies. b

Table 4 Knowledge about HPV infections in different countries (health professionals excluded), reported for 25 studies Question

Heard of HPV…

United Kingdom

Australia

Canada

Brazil

Iceland

South Africa

Germany

Mexico

Belgium

% (reference)

% (reference)

% (reference)

% (reference)

% (reference)

% (reference)

% (reference)

% (reference)

% (reference)

13 (Vail-Smith and White, 1992) 18 (Mays et al., 2000)

30 (Pitts and Clarke, 2002) 31 (Philips et al., 2003) 31 (Waller et al., 2003)

73 (Giles and Garland, 2006) a 93 (Giles and Garland, 2006) b

13 (Dell et al., 2000)

51 (Philips et al., 2005) 51 (Philips et al., 2003)

33 (Giles and Garland, 2006) a 57 (Giles and Garland, 2006) b

10 (Moreira et al., 2006) c

34 (Gudmundsdottir et al., 2003)

68 (Buga, 1998)

1.5 (Klug et al., 2005) d

1.9 (Lazcano-Ponce et al., 2001)

3.1 (Baay et al., 2004)

23 (Hoover et al., 2000)

HPV as a risk factor for cervical cancer was known by… (closed question)

27 (Anhang et al., 2004) 38 (Yacobi et al., 1999) 8 (Vail-Smith and White, 1992) c 13 (Baer et al., 2000) 27 (Yacobi et al., 1999) 39 (Holcomb et al., 2004) 44 (Ramirez et al., 1997) 47 (Pruitt et al., 2005) 49 (Hasenyager, 1999) 53 (Lambert, 2001) 57 (Boardman et al., 2004)

HPV as risk factor for cervical cancer was named by… (open question) Participants who knew that HPV can be asymptomatic

10 (Vail-Smith and White, 1992) 10 (Yacobi et al., 1999)

Participants who knew that HPV is sexually transmitted

27 (Ramirez et al., 1997) 66 (Pruitt et al., 2005) 85 (Lambert, 2001) 47 (Boardman et al., 2004) 70 (Pruitt et al., 2005)

0.6 (Waller et al., 2004) 11 (Pitts and Clarke, 2002) 17 (Pitts and Clarke, 2002)

30 (Pitts and Clarke, 2002)

63 (Giles and Garland, 2006) a 73 (Giles and Garland, 2006) b

83 (Giles and Garland, 2006) b 87 (Giles and Garland, 2006) a

67 (Moreira et al., 2006)

S.J. Klug et al. / Preventive Medicine 46 (2008) 87–98

USA % (reference)

63 (Gudmundsdottir et al., 2003)

84 (Ramirez et al., 1997) a b c d

Women attending local university health service. Women attending cervical dysplasia clinic. Closed question assumed, but not clearly stated. In the publication, 3.2% was given which also included the word “virus”. Here, only “HPV” and “papillomavirus” were considered for comparability with the other studies.

93

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countries were observed, however, no formal statistical test was performed since the numbers of studies were small for most countries, except USA and United Kingdom.

Table 6 Results from three studies on knowledge about HPV infection, stratified for women and men Question

Women Men All p value for difference (%) (%) (%) between men and women (χ2 test) a

Heard about HPV infection of the cervix… (Baer et al., 2000) HPV as risk factor for cervical cancer was selected by… (closed question) (Baer et al., 2000) HPV as risk factor for cervical cancer was named by… (open question) (Waller et al., 2004) Viruses or infection as risk factor for cervical cancer were named by… (Wardle et al., 2001) Participants who knew that HPV is transmitted by skin-to-skin contact during intercourse (Baer et al., 2000) b

35

29

33

16

5

13

Knowledge about HPV and genital warts Knowledge about HPV and genital warts was examined in 13 studies (Table 5). The existence of genital warts was well known among most study participants. More than 88% had heard of genital warts (Ramirez et al., 1997; Mays et al., 2000; Baer et al., 2000; Holcomb et al., 2004), and 5–42% of study participants knew that HPV can cause them (Baer et al., 2000; Holcomb et al., 2004; Boardman et al., 2004; Pruitt et al., 2005; Moreira et al., 2006). Sharpe et al. (2005) found that 45% of women with high-risk HPV infection confirmed that some types of HPV cause genital warts. When asked if there is a relation between genital warts and cervical cancer, 34% answered “no” (Waller et al., 2003), while 2% (Waller et al., 2004) or 10% (Baer et al., 2000) named genital warts or “wart virus” as a risk factor for cervical cancer.

a b

0.9

0.2

Not statistically significant p b 0.05

0.6 Not statistically significant

31

26

29

Not available

23

4

18

p b 0.05

Information in this column was taken from the publications. Only of those who had heard of HPV.

Knowledge of women and men Table 5 Knowledge about HPV and genital warts, reported for 13 studies (health professionals excluded) Question

Answer

Heard of genital warts… Yes No Which STDs can you recall? Does HPV cause genital warts?

Genital warts Yes

Some types of HPV Yes cause genital warts What are the symptoms Warts in women of HPV? Warts in men Genital warts

What do you know about HPV?

How can genital warts be transmitted?

a b c d

% of subjects 88 (Mays et al., 2000) 96 (Baer et al., 2000) 8 (Ramirez et al., 1997) 12 (Holcomb et al., 2004) 15 (Mays et al., 2000) 5 (Moreira et al., 2006) 9 (Baer et al., 2000) a 38 (Holcomb et al., 2004) 42 (Boardman et al., 2004) 42 (Pruitt et al., 2005) 45 (Sharpe et al., 2005) b

83 (Ramirez et al., 1997) 56 (Ramirez et al., 1997) 5 (Vail-Smith and White, 1992) 5 (Pitts and Clarke, 2002) 70 (Giles and Garland, 2006) d 83 (Giles and Garland, 2006) c Warts/warty growth 28 (Holcomb et al., 2004) 30 (Yacobi et al., 1999) Genital warts 8 (Pitts and Clarke, 2002) 22 (Gudmundsdottir et al., 2003) Warts 3 (Pitts and Clarke, 2002) Skin-to-skin contact 63 (Baer et al., 2000) a during intercourse Oral sex 49 (Baer et al., 2000) a Exchange of bodily 42 (Baer et al., 2000) a fluid (blood, semen)

Only students who had heard of genital warts. High-risk HPV positive women only. Women attending local university health service. Women attending cervical dysplasia clinic.

The results of three studies were reported stratified by gender (Baer et al., 2000; Wardle et al., 2001; Waller et al., 2004). Women had better knowledge about HPV than men and knew significantly more often that HPV is a risk factor for cervical cancer (Table 6). Women had heard about HPV infections of the cervix more often and knew significantly more often that HPV is transmitted by skin-to-skin contact (Baer et al., 2000). Knowledge by education Four studies addressed the issue of whether knowledge about HPV infection depends on the educational level (data not shown). The results were inconsistent: while one study found no significant difference (Waller et al., 2003), three others did (Waller et al., 2004; Philips et al., 2005; Moreira et al., 2006). Knowledge and quality of recruitment The recruitment score was applied to 29 studies so that the results could be stratified by quality of recruitment (Fig. 1). A low score for quality of recruiting was found for 12 studies, a medium score for 14 and a high score for 3. Studies with the highest percentage of knowledge scored lower in the recruitment score than the other studies regarding the respective question (Table 7). Knowledge by year of study conduct Linear regression was performed to examine the influence of the year of study conduct on knowledge of HPV infection (Fig. 2). We included six studies of knowledge about HPV as a risk factor for cervical cancer (closed question), which were

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Table 7 Knowledge about HPV infection stratified by recruitment score, reported for 24 studies (health professionals and focus group studies excluded) Question

Heard of HPV…

HPV as a risk factor for cervical cancer was known by… (closed question)

HPV as risk factor for cervical cancer was named by… (open question) Participants who knew that HPV can be asymptomatic

Participants who knew that HPV is sexually transmitted

Low score

Medium score

High score

% (reference)

% (reference)

% (reference)

13 (Dell et al., 2000) 18 (Mays et al., 2000) 23 (Hoover et al., 2000) 73 (Giles and Garland, 2006) a 93 (Giles and Garland, 2006) b 33 (Giles and Garland, 2006) a 39 (Holcomb et al., 2004) 44 (Ramirez et al., 1997) 47 (Pruitt et al., 2005) 49 (Hasenyager, 1999) 53 (Lambert, 2001) 57 (Giles and Garland, 2006) b 68 (Buga, 1998) 3.1 (Baay et al., 2004)

13 (Vail-Smith and White, 1992) 30 (Pitts and Clarke, 2002) 31 (Philips et al., 2003) 31 (Waller et al., 2003) 38 (Yacobi et al., 1999) 8 (Vail-Smith and White, 1992) c 10 (Moreira et al., 2006) c 13 (Baer et al., 2000) 27 (Yacobi et al., 1999) 34 (Gudmundsdottir et al., 2003) 51 (Philips et al., 2003) 51 (Philips et al., 2005) 57 (Boardman et al., 2004) 1.5 (Klug et al., 2005) d 11 (Pitts and Clarke, 2002)

0.6 (Waller et al., 2004) 1.9 (Lazcano-Ponce et al., 2001)

27 (Ramirez et al., 1997) 63 (Giles and Garland, 2006) a 66 (Pruitt et al., 2005) 73 (Giles and Garland, 2006) b 85 (Lambert, 2001) 70 (Pruitt et al., 2005) 83 (Giles and Garland, 2006) b 84 (Ramirez et al., 1997) 87 (Giles and Garland, 2006) a

10 (Vail-Smith and White, 1992) 10 (Yacobi et al., 1999) 17 (Pitts and Clarke, 2002)

30 (Pitts and Clarke, 2002) 47 (Boardman et al., 2004) 63 (Gudmundsdottir et al., 2003) 67 (Moreira et al., 2006)

The recruitment score was applied to 29 studies; however, only the results of 24 studies fitted into the tabular presentation. a Women attending local university health service. b Women attending cervical dysplasia clinic. c Closed question assumed, but not clearly stated. d In the publication, 3.2% was given which also included the word “virus”. Here, only “HPV” and “papillomavirus” were considered for comparability with the other studies.

assigned a medium recruitment quality score, the highest score available in this category. Two studies were excluded due to missing values for year of study conduct (Philips et al., 2003, 2005). The year of study conduct was positively correlated with knowledge, but the correlation was poor (Spearman's correlation coefficient = 0.38) and the p value showed no statistical significance (p = 0.45).

women at a beach, 47% were willing to participate in a trial with three vaccinations (Hoover et al., 2000). In population-based studies, 61% of women were willing to participate (Gudmundsdottir et al., 2003), and 84% of women would allow their adolescent daughter to be immunized in a trial after they had learned of the possibility of preventing cervical cancer (LazcanoPonce et al., 2001).

Confusion with other sexually transmitted infections

Discussion

There was substantial mixing up of HPV with human immunodeficiency virus (HIV) and herpes simplex virus (data not shown) (Ramirez et al., 1997; Yacobi et al., 1999; Dell et al., 2000; Baer et al., 2000; Holcomb et al., 2004; Pruitt et al., 2005). Only 47% and 64% of the participants denied that HPV was related to the “AIDS virus” (HIV) (Ramirez et al., 1997; Pruitt et al., 2005). In two other studies, 20% of the participants thought that herpes was a symptom of an HPV infection and 67% were unsure about it (Yacobi et al., 1999; Holcomb et al., 2004).

In the 39 studies in this systematic review, 13–93% of participants had heard of HPV. Three predictors for knowledge about HPV infections were identified. The first was the type of question asked: in multiple choice (closed) questions, HPV was identified as a risk factor for cervical cancer by 8–68% of participants, while in open questions in which participants were asked to name risk factors for cervical cancer, only 0.6–11% answered “HPV” or “papillomavirus”. The long controversy on use of open or closed questions in surveys was largely resolved in practice in favor of the closed form, which are more efficient for interviewing, coding and analysis (Schuman and Presser, 1979). There are, however, good arguments against closed questions as study subjects are likely to be influenced by the alternative answers given and prone to guessing (Schuman and Presser, 1979; Vinten, 1995). Open questions are preferable if

Willingness to participate in an HPV vaccination trial Willingness to participate in an HPV vaccination trial was examined in three studies. In a convenience sample of young

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Fig. 2. Linear regression was performed for knowledge about “HPV as risk factor for cervical cancer” (closed question) by year of study conduct for six studies with medium level recruitment score.

a group of subjects whose knowledge is unknown or highly variable is investigated (Vinten, 1995). A more valid picture of knowledge is obtained if the subjects must produce an answer themselves (Schuman and Presser, 1979). In this review, only physicians showed a high percentage of knowledge in response to an open question (Martinez et al., 1997; Baay et al., 2006). The second predictor was gender. In three studies in which the results were reported stratified by gender, women had better knowledge about HPV. Additionally, Conaglen et al. (2001) showed that, on a general HPV knowledge score, women scored better than men (p b 0.001). In general, gender differences in health knowledge seem to depend on the topic. In an investigation on a specifically female topic like breastfeeding, women had better knowledge than men (Kang et al., 2005), while men living with HIV in the USA had better knowledge about HIV/ AIDS than women with HIV (Whetten et al., 2004). The third predictor of HPV knowledge was profession since 59–100% of physicians knew about the relation between HPV and cervical cancer. In some of those studies, however, the physicians were selected from large, college-based health centers with an undergraduate student population of at least 3400 (Linnehan et al., 1996) and from among experienced general practitioners with more than 1500 consultations per year, half of them diagnosing patients with sexually transmitted diseases at least monthly (Mulvey et al., 1997). In a study of US clinicians, most knew that HPV infection is common, chronic and often asymptomatic, but many “were unaware of information useful for counseling, e.g. most HPV infections clear spontaneously and wart-and cancer-related HPV genotypes usually differ” (Irwin et al., 2006). In a survey of general practitioners in Norway, most considered it important to inform women about HPV and its involvement in cervical carcinogenesis, but more than half admitted that they had limited knowledge about HPV and did not know where to get up-to-date information (Havnegjerde and

Thoresen, 2004). Moreover, a study among Mexican physicians showed that only 19% knew that HPV types 16, 18, 31, 38 and 45 do not cause genital warts (Aldrich et al., 2005). Selection bias could have led to the high knowledge level of physicians in the studies included in this review, and there may still be a need to provide adequate, up-to-date information about HPV to health professionals globally, especially as they are important mediators of knowledge. Age was not a predictor of knowledge about HPV infection. The results for young women (group 1) and for young men and women (group 3) did not differ from the results for women of all ages (group 2) or women and men of all ages (group 4). Large differences in knowledge were found within the groups of students and patients. However, the group of students consists largely of young people (group 1 and group 3). The response rates of the studies differed from 3% to 100%. In two studies with highest response rates, questionnaires were distributed during class, although there was one populationbased study with a response rate of 86% (Lazcano-Ponce et al., 2001). The response rate is part of the recruitment score, which was applied to examine methodological differences between studies. Several studies with high percentage rates of knowledge had low recruitment scores, and selection bias, due to study design or response rate, might be responsible for some of those high rates. Selection bias might vary between studies, which could explain the large difference in knowledge between studies. The year in which the studies were conducted ranged from 1989 to 2005. As knowledge about HPV infection in the scientific community has increased considerably during this time, knowledge about HPV in the general population might have increased as well. For knowledge about HPV as a risk factor for cervical cancer, year of study conduct was positively associated with the level of knowledge. However, this did not reach statistical significance and the correlation was poor. The analysis was restricted to six studies of medium recruitment score using a closed question. Study limitations and strengths This is, to our knowledge, the first systematic literature review on the topic of knowledge about HPV infection. Our results are important in the era of HPV testing and vaccination. Three predictors of knowledge about HPV infection were identified, and knowledge in different study populations was examined. A recruitment score was assigned to assess the quality of recruitment, and knowledge within different subgroups was investigated. A large number of studies including 19,986 participants were included. The literature search was limited to PubMed and PsyDok databases. Some articles might have been missed because they were published in journals not listed in PubMed or were published in a language other than English. There was a frequent lack of detailed information on response rate, study population and other information in the publications. Some studies showed that willingness to participate in an HPV vaccination trial was quite high; however, we did not

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perform a systematic review on the issue and therefore cannot give a conclusive statement on this topic. The results of the studies were heterogeneous, and the study designs, participants, methods, type of questions and study sizes differed considerably. This might also explain some of the differences in results. These large differences in study designs and knowledge as well as the amount of missing values kept us from calculating pooled estimates, as planned a priori. Conclusions This review shows that public knowledge about HPV infection requires improvement. Providing adequate information to the general public is an important public health issue. HPV vaccination has been taken up, and the introduction of HPV testing into cervical cancer screening is ongoing in some countries. Therefore, it is important that women and men understand the implications of an HPV infection. Schools, the media and health professionals are the main mediators for distributing information about the prevention of cervical cancer, and efforts should be made to improve the quality and frequency of information given to the general public. As men have less knowledge about HPV than women, efforts should be made to include men in educational programs. In the future, better knowledge on the issue is expected because of media coverage of the introduction of HPV vaccination. There is a need for welldesigned, carefully planned and well conducted epidemiological studies in this interdisciplinary area of research. Acknowledgment We thank Dr. Jochem Koenig for discussion of statistical issues. References Ackermann, S., Renner, S.P., Fasching, P.A., Poehls, U., Bender, H.G., Beckmann, M.W., 2005. Awareness of general and personal risk factors for uterine cancer among healthy women. Eur. J. Cancer Prev. 14, 519–524. Aldrich, T., Becker, D., Garcia, S.G., Lara, D., 2005. Mexican physicians' knowledge and attitudes about the human papillomavirus and cervical cancer: a national survey. Sex. Transm. Infect. 81, 135–141. Anhang, R., Wright, T.C., Smock, L., Goldie, S.J., 2004. Women's desired information about human papillomavirus. Cancer 100, 315–320. Arbyn, M., Dillner, J., 2007. Review of current knowledge on HPV vaccination: An appendix to the European Guidelines for Quality Assurance in Cervical Cancer Screening. J. Clin. Virol. 38, 189–197. Baay, M.F., Verhoeven, V., Avonts, D., Vermorken, J.B., 2004. Risk factors for cervical cancer development: what do women think? Sex Health 1, 145–149. Baay, M.F., Verhoeven, V., Peremans, L., Avonts, D., Vermorken, J.B., 2006. General practitioners' perception of risk factors for cervical cancer development: consequences for patient education. Patient Educ. Couns. 62, 277–281. Baer, H., Allen, S., Braun, L., 2000. Knowledge of human papillomavirus infection among young adult men and women: implications for health education and research. J. Commun. Health 25, 67–78. Beatty, B.G., O'Connell, M., Ashikaga, T., Cooper, K., 2003. Human papillomavirus (HPV) education in middle and high schools of Vermont. J. Sch. Health 73, 253–257. Boardman, L.A., Cooper, A.S., Clark, M., Weitzen, S., Whiteley, J.A., Peipert, J.F., 2004. HPV cervical neoplasia and smoking: knowledge among colposcopy patients. J. Reprod. Med. 49, 965–972.

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